citrograph magazine 1 - citrus research … · 10 crb financial report 12 join us at the free...

www.CitrusResearch.org | Citrograph Magazine 1

2 Citrograph Vol. 8, No. 3 | Summer 2017

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PUBLICATION OFFICE

Citrus Research BoardP.O. Box 230

Visalia, CA 93279P: (559) 738-0246F: (559) 738-0607

www.citrusresearch.org

EDITORIAL STAFFGary Schulz, Executive Editor

Ivy Leventhal, Managing EditorMelinda Klein, Ph.D., Science Editor

Mojtaba Mohammadi, Ph.D., Associate Science EditorEd Civerolo, Ph.D., Editorial Consultant

PUBLISHING AND PRODUCTIONCo-Publisher / Project Manager

Carolina M. EvangeloDirector of [email protected]

(209) 777-8995

Co-Publisher / Creative Director/Graphic Designer

Eric Cribbswww.cribbsproject.com

[email protected](559) 308-6277

ADVERTISINGTheresa Machado-Waymire

[email protected](209) 761-4444

Advertising, business andproduction inquiries - call, email

or write us at:Cribbsproject

807 S. Pinkham St.Visalia, Calif. 93292P: (559) 308-6277F: (866) 936-4303

[email protected]

Editorial inquiries - call, emailor write us at:

Citrus Research BoardP.O. Box 230

Visalia, CA 93279P: (559) 738-0246F: (559) 738-0607

[email protected]

SUBSCRIPTIONSUnited States

Single Copies: $4.001-Year Subscription: $15.002-Year Subscription: $28.00

Canada & Foreign1-Year Subscription: $30.002-Year Subscription: $56.00

Send subscription requests to: Citrus Research Board

P.O. Box 230, Visalia, CA 93279

Citrograph is published quarterly by the Citrus Research Board, 217 N. Encina, Visalia, CA 93291. If you are

currently receiving multiple copies, or would like to make a change in your Citrograph subscription, please contact the publication office (above). Every effort is made to ensure

accuracy in articles published by Citrograph; however, the publishers assume no

responsibility for losses sustained, allegedly resulting from following recommendations in this magazine. Consult your

local authorities. The Citrus Research Board has not tested any of the products advertised in this publication, nor has it verified any of the statements made in any of the advertisements. The

Board does not warrant, expressly or implicitly, the fitness of any product advertised or the suitability of any advice or statements

contained herein.

Reproduction or reuse of any photos and/or written material contained within thismagazine is prohibited without the expressed

written consent of the publisher.

On the Cover:"Citrus" is a 4' x 5' original oil painting by Betty Berk, an Expressionist painter living in Visalia, California. Her artwork shows a unique and bold use of color to bring out her love of nature, either in still-life compositions of fruits and flowers or her landscapes and figurative works. Her work may be seen regularly at Cafe 225 on Main Street in Visalia, and will be featured there this year during June, July and the first week of August. Berk works at Dinuba High School and also privately teaches drawing and painting. She is a regular exhibitor at Visalia's Taste the Arts Fair in October; and this November, her art will be featured in the Exeter Courthouse Gallery. Citrus©2014 Betty Berk

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In This IssueSummer 2017 | Volume 8 • Number 3 The Official Publication of The Citrus Research Board

8 Citrus Research Board Nomination Meetings Gary Schulz

10 CRB Financial Report

12 Join Us at the Free Citrus Grower Educational Seminar Series Carolina Evangelo

14 Changing of the GuardIvy Leventhal

16 CRB Researchers Honored Ivy Leventhal

18 Joe Morse: Citrus Researcher Extraordinaire Ivy Leventhal

22 Citrus Showcase Hosts Record-breaking CrowdsCarolina Evangelo

26 California Citrus Holds Strong Thanks to Collaborative Effort Gus Gunderson

28 Notes from the 5th International Research Conference on HLB Melinda Klein, Ph.D., and Carolina Evangelo

32 UC Riverside’s Citrus Day Carolina Evangelo

34 HLB in Guangdong, China Jianchi Chen, Ph.D.

40 Do Broad-spectrum Pesticides Induce Citrus Thrips Damage? Joseph G. Morse, Ph.D., and Elizabeth Grafton-Cardwell, Ph.D.

46 Timing of Adult Fuller Rose Beetle Soil Emergence Joseph G. Morse, Ph.D., et al.

52 Detection of ‘Candidatus Liberibacter’ Infection in California Citrus Darya Mishchuk, Ph.D., et al.

58 ACP Control in Southern California Nastaran Tofangsazi, Ph.D., et al.

62 Phytophthora syringae and New Fungicides for Managing Brown Rot James Adaskaveg, Ph.D., et al.

66 Compatibility of Organic and Conventional Insecticides to Tamarixia radiata Jawwad Qureshi, Ph.D., and Philip Stansly, Ph.D.

Citrograph's mission is to inform citrus producers and other industry members of research progress and results that will help ensure the sustainability of California citrus.

52

62 CORRECTIONThe Spring 2017 Citrograph article,“Comparative Study of Early Detection Techniques: Texas 2 Study” referenced Texas A&M University. The correct reference should have been to Texas A&M University-Kingsville.

46


Citrus Research Board Member List By District 2016-2017 (Terms Expire July 31)

The Mission of the Citrus Research Board:To ensure a sustainable California citrus industry for the benefit of growers by prioritizing, investing in and promoting sound science.

District 1 – Northern California

District 2 – Southern California – Coastal

Member ExpiresJustin Golding 2019Andrew Brown 2019Larry Wilkinson 2019Dan Dreyer 2019Etienne Rabe 2018John Konda 2018Keith Watkins 2018Jeff Steen 2018

Member ExpiresJustin Brown 2018Vacant 2018Jim Gorden 2017Greg Galloway 2017Joe Stewart 2017Franco Bernardi 2017Kevin Olsen 2017

Member ExpiresAlan Washburn 2018John Gless III 2017

Member ExpiresMike Perricone 2017

Member ExpiresMark McBroom 2019

Member ExpiresChris Boisseranc 2019

District 3 – California Desert

Public MemberMember ExpiresVacant 2018

Citrus Research Board | 217 N. Encina St., Visalia, CA 93291PO Box 230, Visalia, CA 93279

(559) 738-0246 | FAX (559) 738-0607E-Mail [email protected] | www.citrusresearch.org

Calendar ofEvents 2017

June 15CCQC Meeting - Bakersfield, California. For more information, visit http://ccqc.org

June 27CRB/UCCE Grower Seminar Series - Exeter Veterans Memorial Building, Exeter, California. For more information, contact the CRB at (559) 738-0246 or visit www.citrusresearch.org

June 28CRB/UCCE Grower Seminar Series - Santa Paula Community Center, Santa Paula, California. For more information, contact the CRB at (559) 738-0246 or visit www.citrusresearch.org

June 29CRB/UCCE Grower Seminar Series - City of Temecula Conference Room, Temecula, California. For more information, contact the CRB at (559) 738-0246 or visit www.citrusresearch.org

July 12CPDPC Meeting - Visalia, California. For more information, visit https://www.cdfa.ca.gov/citruscommittee/

August 3CCQC Meeting - Bakersfield, California. For more information, visit http://ccqc.org

August 8CCQC and CRB Joint Executive Committee Meeting - CRB office, Visalia, California.For more information, visit http://ccqc.org

August 14-18 Citrus Research Board Meeting and HLB External Review - Davis, California. For more information, contact the CRB at (559) 738-0246 or visit www.citrusresearch.org

September 13CPDPC Meeting - Riverside/San Bernardino, California. For more information, visit https://www.cdfa.ca.gov/citruscommittee/

September 26 Citrus Research Board Annual Meeting - Lindcove Conference Room, Exeter, California. For more information, contact the CRB at (559) 738-0246 or visit www.citrusresearch.org

October 11 California Citrus Conference - Wyndham Hotel, Visalia, California. For more information, contact the CRB at (559) 738-0246 or visit www.citrusresearch.org


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Citrus Research Board Nomination MeetingsBy Gary Schulz, President, Citrus Research Board

California citrus producers in District 1 and 2 should make plans to attend the appropriate nomination meetings for

the Citrus Research Board (CRB). Five positions in District 1 expire on July 31, 2017, and there is one vacancy to be filled that will subsequently expire in 2018. Two positions in District 2 expire on July 31, 2017. The public nomination meetings will be conducted by officials of the California Department of Food and Agriculture (CDFA).

In addition to the elected positions mentioned above, the Board will have the opportunity to fill the vacant public member position at its annual meeting on September 26, 2017.

The detailed list of seats expiring in 2017 and other vacant positions may be found on page 6, where the current board member roster appears by name, district and year of the term’s expiration. Member terms are for three years.

Board Member ResponsibilitiesThe bulk of the Board’s time is spent considering a broad portfolio of citrus research proposals and projects totaling millions of dollars. Members are involved in developing research priorities, Requests for Proposals, prioritizing responses, awarding funds, devising successful implementation strategies, assessing progress and providing critiques of project results. The 21-member Citrus Research Board is served by a 13-member staff with offices in Visalia and Riverside.

There is a relatively high time commitment compared to many other volunteer commodity boards, but those involved with the CRB are integral in directing the response to critical citrus research needs in California. Board members are expected to attend Board meetings and to serve on research and/or administrative committees. A typical fiscal year has five Board meetings in various geographic locations, two three-day research meetings to receive project updates and several committee meetings. Board members also have the opportunity to attend a number of citrus-related conferences and events.

District 1Northern California Region2 p.m., Monday, June 19, 2017Tulare County Ag Commissioners Conference Room4437 Laspina Street, Tulare, California 93274559-684-3350

District 2Southern California - Coastal Region2 p.m., Tuesday, June 20, 2017Santa Paula Community Center530 West Main StreetSanta Paula, California 93060


Board Member Qualifications (as provided by the CDFA Marketing Branch):• Any owner, officer or employee of an entity in California

in the business of producing, or causing to be produced for market, 750 or more standard field boxes (or the equivalent) of any variety of citrus is qualified to participate in the nomination proceedings.

• An individual person is entitled to represent only one legal entity at a nomination meeting.

• In the case of a partnership, only one of the partners may vote.

• In the case of a corporation, a person affiliated with the corporation, preferably an officer, may represent the corporation.

• A married couple operating a production entity is entitled to just one vote, unless each spouse owns and operates separate and distinct entities.

• To participate in a district’s nomination meeting, a business entity must have citrus production within that district. Any entity with production in more than one district must choose a single district in which to participate to vote. If a separate production entity can be proven as the operating entity in another district, the person qualified to act as the representative of that entity may vote in that district, even if he/she has voted as a representative of another entity in another district. Essentially, each separate citrus-producing business entity is entitled to one vote in the district in which it operates.

• Voting by proxy is not permitted.

For more information you may view the California Citrus Research Program Marketing Order at:http://www.cdfa.ca.gov/mkt/mkt/pdf/Laws/CitrusResearchMarketingOrder.pdf

Questions may be directed to Robert Maxie, CDFA Marketing Branch Chief, 916-900-5179; Kacie Fritz, CDFA Associate Agricultural Economist, 916-900-5095; or Gary Schulz, CRB President, 559-738-0246.

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9,862,256

CRB FINANCIAL POSITIONAs of

9/30/2014As of

9/30/2015As of

9/30/2016Assets 6,809,954$ 5,773,695$ 7,638,035$ Liabili�es 1,098,450$ 633,968$ 2,260,140$ Net Assets 5,711,504$ 5,139,727$ 5,377,895$

SUMMARY OF ACTIVITIES For the year

ended 9/30/14

For the year ended

9/30/15

For the year ended

9/30/16 IncomeAssessment Rate $ 0.041 $ 0.040 $ 0.040

Assessment Income 7,177,455$ 7,379,405$ 8,419,169$ CPDPP Grant Income 1,609,067 782,168 783,581$ Federal Grant Income 967,105 852,738 1,326,792$ Investment Income 62,812 44,997 40,937$ Other Income 45,817 174,461 179,257$

9,233,769 10,749,736$ $ $

ExpensesResearch Expenses 6,807,002 7,496,343 7,805,635$ Opera�ons Expenses 1,058,952 745,289 723,458$ Communica�on Expenses 310,137 143,448 185,618$ Administra�ve Expenses 1,239,601 1,405,761 1,349,003$ Other Expenses 473,861 14,706 501,559$

9,889,553 9,805,547 10,565,273$

Increase (Decrease) in Net Assets (27,297)$ (571,778)$ 184,463$

Total Income

Total Expenses

$ $ $ $ $ $

$ $ $ $ $ $

The above table lists the audited financial statement of the Citrus Research Program for the years ended September 30, 2014, 2015 and 2016. A complete copy of the audit is available for viewing at the CRB office at 217 North Encina in Visalia, California. You are welcome to visit us at any time to discuss any elements of the program and see what we are doing. This program is paid through your assessment dollars, and the Board welcomes your feedback. –Gary Schulz, President, Citrus Research Board

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Join us at theCITRUS GROWERS EDUCATION SEMINAR SERIES

Presented by Citrus Research Board and UC Cooperative Extension

TUESDAY, JULY 15California Citrus State Historic Park,

Riverside 9400 Dufferin Ave.Riverside, California 92504

8:30 A.M. – NOON

THURSDAY, JULY 17Exeter Veterans Memorial Building

324 N Kaweah AveExeter, California 93221

8:30 A.M. – NOON

Agenda and details at www.citrusresearch.org

No registration fee, but RSVPs are appreciated! Please call the Citrus Research Board at (559) 738-0246 or email: [email protected] at your earliest convenience.

Join us at the Citrus Growers Educational Seminar Series

Presented by the Citrus Research Board and University of California Cooperative Extension

Central CoastSanta Paula, California

Wednesday, June 28Santa Paula Community Center530 W. Main StreetSanta Paula, California 93060

Registration: 7:30 amSeminar: 8:00 am – Noon

SPEAKERS AND TOPICSBen Faber, Ph.D., UCCE Citrus Advisor -Regional citrus update

Beth Grafton-Cardwell, Ph.D. – Director of Lindcove REC and Research Entomologist, University of California, Riverside -Management strategies for Asian citrus psyllid

Joe Morse, Ph.D. – University of California, Riverside-Dr. Morse’s final CRB talk in Santa Paula: Past and present review of Integrated Pest Management (IPM) and thoughts on the future

Ed Stover, Ph.D. – USDA-ARS, Fort Pierce, Florida-Breeding citrus for HLB tolerance/resistance

Carol Lovatt, Ph.D. – University of California, Riverside-Alternate bearing

Southern California – DesertTemecula, California

Thursday, June 29City of Temecula Conference Room41000 Main StreetTemecula, California 92590


SPEAKERS AND TOPICSGary Bender, Farm Advisor Emeritus-Subtropical Horticulture-Regional citrus update

Beth Grafton-Cardwell, Ph.D. – Director of Lindcove REC and Research Entomologist, University of California, Riverside -Management strategies for Asian citrus psyllid

Joe Morse, Ph.D. – University of California, Riverside-Dr. Morse’s final CRB talk in Temecula: Past and present review of Integrated Pest Management (IPM) and thoughts on the future


Carol Lovatt, Ph.D. – University of California, Riverside-Alternate bearing and late season lemon drop issues in the desert

Central ValleyExeter, California

Tuesday, June 27Exeter Veterans Memorial Building324 N. Kaweah AvenueExeter, California 93221


SPEAKERS AND TOPICSGreg Douhan, UCCE Citrus Advisor, and Beth Grafton-Cardwell, Ph.D. – Director of Lindcove REC and Research Entomologist, University of California, Riverside -Regional citrus update

Beth Grafton-Cardwell, Ph.D. – Director of Lindcove REC and Research Entomologist, University of California, Riverside - Management strategies for Asian citrus psyllid

Joe Morse, Ph.D. – University of California, Riverside- Dr. Morse’s final CRB talk in Exeter: Past and present review of Integrated Pest Management (IPM) and thoughts on the future


Carol Lovatt, Ph.D. – University of California, Riverside-Alternate bearing CONTINUING EDUCATION UNITS WILL BE AVAILABLE, PENDING APPROVAL BY THE CALIFORNIA

DEPARTMENT OF PESTICIDE REGULATION.

PLEASE CALL THE CITRUS RESEARCH BOARD AT (559) 738-0246 OR EMAIL: [email protected] AT YOUR EARLIEST CONVENIENCE.WATCH FOR MORE DETAILS AT WWW.CITRUSRESEARCH.ORG

FREE, NO REGISTRATION FEE, BUT RSVPS ARE APPRECIATED.

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Changing of the GuardJim Gorden Named Citrus Research Board ChairmanIvy Leventhal

Citrus veteran and pest management pioneer Jim

Gorden was elected chairman of the Citrus Research Board (CRB) at a meeting of the Board on February 8, 2017. He is completing the term of Richard Bennett, who stepped down from the helm on January 20. Gorden previously had served as CRB chairman in 2009-11.

“We deeply appreciate Jim’s leadership, his commitment to the California citrus industry and his dedication to citrus research,” said CRB President Gary Schulz. “Jim’s past experience as CRB chairman, his long-time service on the Board and his keen knowledge of the California citrus industry are all tremendous assets to our organization.”

Gorden will serve as chairman until the CRB’s annual meeting on September 26, 2017. Continuing their service as officers are Vice-Chair Dan Dreyer and Secretary-Treasurer John Konda.

“On behalf of the Board, I’d like to thank Richard Bennett for his energy, enthusiasm and passion for citrus research and the California citrus industry,” Gorden said. “I’d also like to express my appreciation to Dan Dreyer for filling in as interim chairman. I’m looking forward to guiding the CRB through this important period as we seek to find solutions to the critical threat of huanglongbing that’s looming over our industry.”

Gorden’s primary areas of professional involvement have been integrated pest management, horticulture and a broad range of citriculture, and he is a recognized international expert in

those fields. For more than 35 years, he was a partner in in Pest Management Associates, which was the first independent citrus pest management consulting company providing service to the San Joaquin Valley.

“I’ve always been interested in science, research and horticulture,” Gorden said. “and I became more heavily involved in farming after I withdrew from consulting.” As a result, his farming business has grown over the last ten years.

The Lemon Cove resident holds a bachelor’s degree in biology from California State University, Fresno. He and his wife, Mary, have supported youth activities such as 4-H and the Boys and Girls Club in Exeter. Gorden also serves or has served with many civic and professional organizations. He has worked with the California Citrus Pest and Disease Prevention Program since its inception and continues to remain heavily involved. Additional activities include eight years with the California Citrus Nursery Board, as well as working with the ACP/HLB Task Force, Southern Sierra Archeological Society, Central California Tristeza Eradication Board, Chair of the Tulare County Pest Control District, the Association of Applied Insect Ecologists and ten years on the local school district board.

Gorden and his wife, Mary, have been married for 53 years and have five grandchildren. Their son, Milo, is married to Elia and is a partner in running the farms. Their daughter, Megan, and her husband, Sean, also are partners in some of the Gorden operations.

Ivy Leventhal is the managing editor of Citrograph. For further information, contact [email protected].


Three California-based Citrus Research Board (CRB) researchers recently have received important recognition for their work to find solutions for citrus pests and diseases.

Michelle (Cilia) Heck, Ph.D., a research molecular biologist for the USDA-Agricultural Research Service (ARS) at the Robert W. Holley Center in Ithaca, New York, was named a recipient of the Presidential Early Career Awards for Scientists and Engineers (PECASE). The recognition is the highest honor bestowed by the U.S. government on science and engineering professionals

in the early stages of their independent research careers. Heck's group is working to develop an early huanglongbing (HLB) detection method through identifying proteins generated by citrus trees soon after infection. They also are using a chemical cross-linking mass spectrometry technology (developed by collaborators in the Bruce Lab at the University of Washington) to study the protein interactions that regulate transmission by the insect vector.

The PECASE awards, established in 1996, highlight the emphasis that the White House places on encouraging and accelerating American innovation to grow the economy and tackle the greatest challenges. Researchers are selected for their pursuit of innovative research at the frontiers of science and technology and their commitment to community service as demonstrated through scientific leadership, public education or community outreach. Heck was one of three honored in the agriculture sector.

Former President Barak Obama, who bestowed the award in January, said, “I congratulate these outstanding scientists and engineers on their impactful work. These innovators are working to help keep the United States on the cutting edge, showing that Federal investments in science lead to advancements that expand our knowledge of the world around us and contribute to our economy.”

Elizabeth Grafton-Cardwell, Ph.D., is a citrus integrated pest management (IPM) specialist at the University of California, Riverside (UCR) and also serves as director of the Lindcove Research and Extension Center in Exeter, California. This past February, she received the Lifetime Achievement Award from the Association of Applied IPM Ecologists (AAIE) at their annual

conference in Napa, California. This association’s 200-plus members lead the development, adoption and implementation of IPM, an area where Grafton-Cardwell has played a leading role. The award recognized Grafton-Cardwell for her 26 years of contributions to the integrated pest management of California citrus.

“I study insect pests of citrus in the central San Joaquin Valley and develop integrated methods of pest control,” Grafton-Cardwell said, adding, “I study the life cycles of these pests and how to sample for them, how to preserve and boost their natural enemies and how to utilize pesticides in ways that minimizes their use.” Grafton-Cardwell’s work is important because “it provides citrus growers with the most effective methods to keep pest populations under control and minimizes fruit damage so that growers can provide affordable, healthy fruit to consumers.” (Grafton-Cardwell is a co-author of three articles in this issue – “Pesticide-induced Stimulation of Citrus Thrips” on page 40, “Timing of Adult FRB Soil Emergence” on page 46 and “ACP Control in Southern California” on page 58.)

The third honoree is Jianchi Chen, Ph.D., a research molecular biologist at the USDA-ARS San Joaquin Agricultural Sciences Center in Parlier, California. Last fall, Chen received a Certificate of Appreciation from the USDA “in recognition of outstanding support in assisting PPQ CPHST (Plant Protection and Quarantine Center for Plant Health Science and Technology)

Beltsville Laboratory with the diagnoses of plant pathogen huanglongbing (HLB).”

A bacteriologist, Chen explained that his current work focuses on studying “fastidious prokaryotes, which are bacterial pathogens that are difficult to culture or are not culturable, such as Xylella, ‘Candidatus Liberibacter species’ and ‘Candidatus Phytoplasma species’ through traditional and genomic approaches.” (Chen’s article, “HLB in Guangdong, China” may be found on page 34 of this issue.)

“We are proud of all of the scientists who pursue their important research in partnership with the CRB,” said CRB President Gary Schulz. “However, we’re especially proud to see our researchers honored by the U.S. government and other key organizations for their critical work on HLB and other diseases and citrus pests.”

Ivy Leventhal is the managing editor of Citrograph. For more information, contact [email protected].

CRB Researchers HonoredIvy Leventhal


Joe Morse: Citrus Researcher ExtraordinaireIvy Leventhal

After 36 years devoted to conducting scores of highly significant and important research projects on behalf of the California citrus growers, University of California, Riverside (UCR)

Professor of Entomology and Entomologist Joseph G. Morse, Ph.D., is hanging up his lab coat this July and looking forward to a well-deserved retirement.

“After all these years of dedicated citrus research, I know I speak for the entire California citrus industry in wishing Joe Morse a long, healthy and happy retirement. He has made a

difference in the lives of many citrus growers,” said Gary Schulz, president of the Citrus Research Board (CRB).

The holder of a B.S in Electrical Engineering/Biology from Cornell University and an M.S. in Systems Science, M.S. in Entomology and Ph.D. in Entomology, all from Michigan State University, the Ithaca, New York, native had never been west of Michigan until he accepted his first job at UCR in 1981 several months before receiving his Ph.D.

Morse giving a talk to citrus growers in the field.

Joe Morse, Ph.D.


“On my second day on the job, I traveled to the San Joaquin Valley to visit the Lindcove Research and Extension Center (LREC) and also met with Neil Fisher, then-president of the CRB, who ‘demanded’ that I put in a research proposal to work on citrus thrips,” Morse said. “I did this in November 1981 and have conducted CRB-funded research on citrus thrips and other pests continuously ever since.”

Morse became a researcher, educator, administrator and author. The bulk of his efforts through the years at UCR focused on citrus and avocado pest management, biological control, chemical control, pesticide resistance management, phytosanitary security and risk analyses. The “fruits” of his research results have helped ensure the economic viability of California’s citrus industry.

“I have tried to return value to the citrus and avocado industries, both of which have been extremely supportive of my research efforts

through the years,” Morse said. “The funding they provided was very helpful; but more than that, I have valued the positive support and the interest of growers and pest control advisors in working with me to solve real-world issues, and also all the friendships I have made. I feel like the citrus and avocado industries have given me every bit as much as I have given them, if not more.”

Mary Lu Arpaia, Ph.D., UCR extension subtropical horticulturist and a long-time associate of Morse said, “Joe Morse epitomizes commitment, excellence and dedication to the mission of the University of California and the Citrus Experiment Station as demonstrated by his many years of service. He always has been fully committed to helping the California citrus industry and responsive when problems arose.” Arpaia added, “He is a rigorous scientist. Joe has never cut corners in his research. He always made certain to adhere to a high level of scientific rigor to ensure that his results were based in sound experimental design and applicable to all end-consumers. For that, I am very honored to have worked and been associated with Joe throughout his career at UCR.”

The results of Morse’s research have been prolific. His work has appeared in several hundred publications, including 49 reports published over the years in Citrograph (Editor’s note: see articles in this issue on pages 40 and 46).

Morse said, “I have interacted with a lot of commodity boards and commissions in California and elsewhere, and the CRB has been the best. I think it is because citrus growers must take a long-term perspective as much as anyone in agriculture. They have

to meet the bottom line each year; but still, it is many years after planting before returns become positive and, if you maintain a healthy grove, it is highly productive for a long time.”

“Although Board members might disagree on a specific research issue, they all clearly see the value of research,” he added, “or they wouldn’t spend all the time they do serving gratis on the Board, which is a big investment of time by obviously successful people. I have been truly grateful for their support.”

MaryLou Polek, Ph.D., research leader and research plant pathologist at the USDA-Agricultural Research Service National Clonal Germplasm Repository for Citrus and Dates, has known Morse for many years. “He always has been a strong advocate for citrus growers,” she said. “Joe’s contributions toward the development and implementation of IPM programs for pest control will continue to benefit the industry and

Joe Barcinas and Morse on one of their fishing trips in Cabo San Lucas, Mexico.


environment for many years to come. While an outstanding scientist, he also has the ability to understand everyday farming problems, develop practical tools and strategies and convey knowledge to growers.”

Another of the many colleagues who will miss Morse tremendously is Beth Grafton-Cardwell, Ph.D., an extension specialist at UCR and director of the LREC. “Joe Morse and I worked together for many years, attempting to solve both new and old pest problems of California citrus,” she said. “Joe’s research established the basis for the current citrus thrips and avocado thrips management programs. He also took a special interest in pests of export significance, notably bean thrips and Fuller rose beetle, studying their biology and developing most of the mitigation strategies that growers are using today. Joe always made himself accessible to the citrus industry and to researchers like myself.”

The renowned scientist’s numerous awards include the following:• Elected Fellow, Entomological Society of America• Albert G. Salter Memorial Award, California Citrus Quality Council• Award for Excellence in Integrated Pest Management,

Entomological Society of America• Award of Honor, California Avocado Society• Elected Fellow, American Association for the Advancement of

Science• Art Schroeder Memorial Award, California Avocado Society• Award of Excellence, Citrus Research Board• Recognition Award in Entomology, Entomological Society of

America

On July 1, Morse, an avid fisherman, will move to New Hampshire to share a lake house with his sister for four or five months annually. It

is a region he is familiar with, having spent most of his summers in that area while growing up. The remainder of the year, Morse will live in Nichada Thani, Thailand, an ex-pat community of roughly 3,000, located about 20 miles north of Bangkok, close to his sister’s family.

Grafton-Cardwell spoke for many people when she said, “I will miss Joe’s wealth of knowledge, experience, insights and enthusiasm for IPM problem solving.”

“The university has a great challenge before them to find a replacement with such talents,” Polek added.

The California citrus community thanks Joe Morse for his many years of dedicated service and wishes him an enjoyable retirement.

Ivy Leventhal is the managing editor of Citrograph. For more information, contact [email protected]

Barcinas and Morse showcasing pests on citrus.

Heavenly Clegg, Joe Morse, Pam Watkins, Alan Urena and Lindsay Robinson.


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Previous crowd records fell as more than 1,500 members of the citrus industry attended the 2017 Citrus Showcase on

March 2 at the Visalia Convention Center. Another record was set with 134 trade booths.

Tracy Kahn, Ph.D., University of California, Riverside (UCR), and Rock Christiano, Ph.D., Lindcove Research and Extension Center (LREC) were instrumental in their assistance with this year’s Citrus Research Board (CRB) exhibit, curating the fruit display and greeting attendees to educate them about the different citrus varieties in the booth. The display showcased 25 different new varieties grown at UCR and LREC facilities. Additionally, Integrated Pest Management expert Beth-Grafton Cardwell, Ph.D., and University of California Cooperative Extension (UCCE) farm advisors Craig Kallsen and Greg Douhan were available to answer grower questions.

During the showcase, California Citrus Mutual (CCM) and the CRB conducted six free seminars. A brief recap of each of these seminars follows.

Farming a Way Through California’s Groundwater MazeCCM Director of Government Affairs Laura Brown began the morning workshops with a convincing argument on why the drinking water quality issue was not just a nitrate issue nor simply a result of farming practices. Westside grower and water attorney David Cory provided a historical overview of the Central Valley Salinity Coalition’s work on CV-SALTS (a collaborative stakeholder program to address the long-term build-up of salts and nitrate issues in the Central Valley) and why it is going to be important in the shaping of groundwater quality policy in the future. Growers also heard from Kaweah Basin Water Quality Association Executive Director Donald

Citrus Showcase Hosts Record-breaking CrowdsCarolina Evangelo

Tracy Kahn, Ph.D., discussed the citrus variety display with a Showcase attendee.


Ikemiya on what they need to do to comply with the Irrigated Lands Regulatory Program requirements.

Genome Targeting for Precise DNA ModificationCRB researcher James Thomson, Ph.D., USDA-Agricultural Research Service (ARS), discussed ongoing CRB-funded research into the Recombinase Mediated Cassette Exchange (RMCE) technology as a means to add specific traits of interest to popular California citrus scion and rootstock varieties. Thomson also explained the genetic engineering process to generate transgenic citrus plants with novel, beneficial traits, including incorporation of huanglongbing (HLB)

resistance traits. Concept and commercialization possibilities of marker removal available with this approach also were highlighted.

First Line of Defense – Coordinated Area-wide Programs Grafton-Cardwell and CCM Chairman Curt Holmes presented a detailed overview of the proposed coordinated area-wide spray program and discussed why it will be essential in controlling Asian citrus psyllid (ACP) populations and slowing the spread of HLB. Curt talked about his experience as a team captain in his psyllid management area (PMA) and encouraged growers to step up to captain a PMA when needed.

Protecting the California Citrus Industry from Invasive Pests at US Ports of Entry and Borders

CRB-sponsored speaker Nicki Thomas, Agriculture Programs and Trade Liaison (APTL) of U.S. Customs and Border Protection (CBP), gave an update on what the CBP is doing to keep invasive pests from crossing US borders, especially in the west. Thomas highlighted the excellent K-9 officers on the CBP team and gave an overview of the types of plant materials and goods that K-9 officers have intercepted while on duty.

An Evaluation of Industry Efforts to Stop HLBAfternoon workshop attendees viewed a live demonstration of an automated tarping system that allows the operator to stay on the ground while tarping his citrus load. Spencer Walse, Ph.D., USDA-ARS, and Dave Sorenson of Fruit Growers Supply demonstrated a fogging system that utilizes Evergreen® to kill ACP in loaded bins in the field before they move to the packinghouse. The system is envisioned to be an alternative to wet washing.

Sold-out Luncheon ProgramThis year’s luncheon program drew a sold-out crowd of approximately 800 guests and featured a panel discussion led and moderated by CCM President Joel Nelsen. Distinguished

James Thomson, Ph.D., Crop Improvement and Genetics Research Scientist at USDA-ARS, discussed the latest technologies being developed to combat HLB.

Nicki Thomas, Agriculture Programs and Trade Liaison (APTL) of U.S. Customs and Border Protection (CBP), delivered a talk to seminar attendees.

Luncheon panelists featured Berne Evans, CEO of Sun Pacific; Jim Marderosian, president of Bee Sweet Citrus; Joel Nelsen, CCM President and panel moderator; David Krause, president of Wonderful Citrus; and Russ Hanlin, CEO of Sunkist Growers.


panel members included California packinghouse leaders David Krause, president of Wonderful Citrus; Berne Evans, CEO of Sun Pacific; Jim Marderosian, president of Bee Sweet Citrus;

and Russ Hanlin, CEO of Sunkist Growers. Panelists had a frank conversation about the California citrus industry and the challenges it faces. The entire panel agreed that great quality products always enjoy high demand in the marketplace.

HLB was discussed, including concerns about the huge impact it has had in other citrus industries around the world. Although HLB is considered the number one enemy in the citrus industry, the issue of water in California shares “highest priority” status for all four panelists. They believe more pressure needs to be put on state and federal legislatures to help solve the California water crisis. Without water, there will be no citrus industry.

Carolina Evangelo is the CRB director of communications and the co-publisher/project manager of Citrograph. For more information, contact [email protected]

Greg Simmons, Ph.D., USDA-APHIS; Nawal Sharma, California Department of Food and Agriculture; and Tom Delfino, executive director of the California Citrus Nursery Society, visited about characteristics one of the new citrus varieties on display.

Raul Gonzalez, retired LREC employee; Rick Dunn, CRB data management director; and Beth Grafton-Cardwell, Ph.D., director of Lindcove REC and research entomologist, University of California, Riverside, chatted at the CRB booth.


Committed to winning the fight against huanglongbing (HLB), California citrus growers began funding the Citrus Pest & Disease

Prevention Program (CPDPP) in 2008 when the Asian citrus psyllid (ACP) was first discovered in San Diego County. Today, the industry continues to reap the rewards of this investment, as the disease has been kept out of commercial groves.

Since the first discovery of HLB in the Hacienda Heights area of Los Angeles County in 2012, 56 citrus trees in the state (as Citrograph was going to press) have tested positive for the fatal tree disease – all residential trees that were promptly destroyed. Compare this to Florida: once the disease was discovered in south Florida in 2005, it only took a little more than two years for the disease to spread to all the citrus-producing regions in the state.

According to a University of Florida study conducted four years ago, the disease caused more than $4 billion in economic damage, including the elimination of 8,000 jobs. Today, Florida Citrus Mutual estimates those numbers have doubled.

While the presence of HLB in California is disheartening to say the least, our industry is still thriving. In large part, this is because of the citrus industry’s diligence in acting early to address the pest and

disease. Through the CPDPP, California citrus growers are buying time for researchers to develop a long-term solution for HLB. These aggressive tactics are crucial to the future of California citrus.

Urban Pest ResponseFlorida growers have said that their biggest error was not addressing ACP control when the pest was first discovered in Florida in 1998. By the time disease symptoms showed up on trees, the state was infested. Therefore, a major component of the CPDPP is a residential detection and treatment program implemented by the California Department of Food and Agriculture (CDFA). Psyllid control in California has been our number one defense since the pest was discovered here.

Traps are deployed throughout the state, and the public is encouraged to report potential psyllid detections through a free state hotline, which is promoted via the CPDPP outreach program. When the psyllid was first discovered in California and pest populations were minimal, the CPDPP handled every pest detection with aggressive treatments. As populations of the pest increase in the state, the program has diversified its efforts to also include the rearing and release of biological control agents, and has shifted its treatment

California Citrus Holds Strong Thanks to Collaborative EffortGus Gunderson

CDFA staff inspects a backyard citrus tree as a part of the Citrus Pest & Disease Prevention Program’s residential program.


strategy to areas most at risk for the disease or near commercial citrus operations.

Disease Detection and EradicationBased on research, a system was developed to estimate the likelihood of HLB presence in various areas. The CDFA routinely conducts HLB risk-based surveys throughout the state. The system considers numerous factors to determine risk of disease exposure, including proximity to other diseased trees, density of citrus in the area and proximity to transportation corridors, and it helps the CDFA focus resources on areas most at risk.

Highly trained CDFA contractors collect samples of plant material and collect psyllids, if the pest is present, from host plants. In 2016, the CDFA collected nearly 50,000 plant samples and nearly 80,000 ACP samples to test for HLB. Since sample collection began in 2008, more than 400,000 plant and psyllid samples have been collected and processed.

If a tree tests positive for the HLB-associated bacterium, 'Candidatus Liberibacter asiaticus' via the USDA-approved PCR diagnostic test, the tree is removed and destroyed immediately. Tree removal is mandatory – homeowners cannot opt out. Fortunately, most residents see the value in protecting California’s citrus industry and the citrus trees in their community, and readily agree to prompt tree removal. Additionally, all host plants within 800 meters around an HLB detection site are treated and receive intensive visual survey. Treatments and visual surveys also are mandatory. The CDFA continues to treat properties in HLB-find site areas on a routine basis.

Protecting Commercial Citrus CommunitiesYet another lesson learned from Florida, was the importance of growers coordinating their ACP treatments for maximum impact on pest populations. To curb those pest populations and scout for the disease in California’s urban areas, the CPDPP provides a framework for the industry to best manage the threat in their groves. The CPDPP worked with researchers and other industry leaders to develop a treatment plan and also hired liaisons to advise growers on the timing of coordinated and area-wide applications.

To maximize the impact of area-wide treatments, the CDFA will treat residential properties located within 400 meters around commercial properties that are participating in an area-wide management program. This only happens, however, if 90 percent of commercial citrus in the treatment area is participating. It is imperative that growers work together to receive a true area-wide effect.

The CPDPP is actively engaging all available resources to stay one step ahead of HLB. We urge you to stay engaged with the program by attending committee meetings and providing feedback when new strategies are being explored. Visit CitrusInsider.org to sign up for news alerts and view upcoming meeting dates. By working together, we can save California citrus.

Gus Gunderson is chairman of the outreach subcommittee, Citrus Pest & Disease Prevention Program. For more information, contact [email protected]

A look at the decline in Florida citrus production due to diseases like HLB and citrus canker, hurricanes and other factors. Data were gathered from USDA-National Agricultural Statistics Service, and are accurate as of March 2016.


Melinda Klein and Carolina Evangelo

Notes from the 5th International Research Conference on HLBA Week of Tours, Talks and Troubles to Come

This past March, the best place to see just how far-flung the reach of huanglongbing (HLB) has been and the breadth of the research underway to combat it was at the 5th International Research Conference on Huanglongbing (IRCHLB) in Orlando, Florida. A contingent of Citrus Research Board (CRB) members, staff and funded researchers were in attendance to learn the latest news on research efforts, present their findings, confer with current collaborators and make new connections with researchers from around the world to identify solutions to this deadly disease. When the 5th IRCHLB was held in Orlando, March 14-17, the conference welcomed nearly 500 participants from more than 24 countries with three days of presentations focused on the disease, including the three organisms involved:• ‘Candidatus Liberibacter asiaticus’ (CLas) – the bacterial

pathogen presumed responsible for HLB, • Asian citrus psyllid (ACP) – the leafhopper insect that

spreads (vectors) CLas and • Citrus – the host plant and unlucky victim in this disease

triangle.

The role of each of these organisms in the epidemiology of the disease – biology, interactions, rates and methods of CLas spread in the field, the role of cultural practices and treatments in slowing the spread of infection or limiting the effect of the disease in trees, and breeding efforts to identify tolerant or resistant varieties – were reviewed in depth at the conference. Current and former CRB Board members in attendance included Chairman Jim Gorden, Vice-Chairman Dan Dreyer, Past Chairman Etienne Rabe, Ph.D., Secretary-Treasurer John Konda, Justin Golding, Greg Galloway and Past Chairman Richard Bennett. CRB staff and consultants in attendance

IRCHLB Conference Chairman and USDA-ARS’s Tim Gottwald, Ph.D. opens the conference with a welcome address.


CRB Board Member John Konda and his wife, Maryanne.

Sandy Olkowski, Ph.D., who is working with David Bartels, Ph.D., and Neil McRoberts, Ph.D., at UC Davis on modeling the changes in the CLas qPCR values in the psyllid samples collected in the risk-based survey, as part of a USDA HLB Multi-Agency Coordination Group grant; CRB Chief Research Scientist Melinda Klein, Ph.D., and Sara Garcia Figuera, a graduate student in McRoberts' group. Garcia Figuera arrived in Davis from Madrid last fall and is a Fulbright Scholar studying regulatory and strategic issues in HLB management. She is working with McRoberts on modeling expected outcomes of grower cooperation to control HLB.

Dawn Streich, Givaudan Flavor Corporation; Chad Hansen, Givaudan Flavor Corporation; and Tracy Kahn, Ph.D., UC Riverside.

CRB Vice-Chairman Dan Dreyer, CRB Board Member Keith Watkins and his wife, Susan.

CRB Chairman Jim Gorden, CCM Board Member John Gless, Raul Garcia of Gless Ranch, CRB Board Member Etienne Rabe, Ph.D. and CRB Board Member Justin Golding.

FruitMentor’s Dan Willey; UCR Researcher Chandrika Ramadugu, Ph.D.; CRB Chairman Jim Gorden and CRB Associate Scientist Mojtaba Mohammadi, Ph.D.

included President Gary Schulz; CRB Advisor Ed Civerolo, Ph.D.; Chief Research Scientist Melinda Klein, Ph.D.; Associate Scientist Mojtaba Mohammadi, Ph.D.; Director of Field Operations and Biological Control Lead Raju Pandey, Ph.D.; Jerry Dimitman Laboratory Director Cynthia LeVesque, Ph.D.; and Director of Communications Carolina Evangelo. Seventeen CRB-funded principal investigators and/or key staff members also attended and presented their work to the research audience.

Prior to the start of the conference, educational tours were set up for Board members by Philippe Rolshausen, Ph.D., and Richard Bennett to visit a citrus under-cover protection system (CUPS) run by Arnold Schumann, Ph.D., at the University of Florida Citrus Research and Education Center Lake Alfred Experiment Station in Lake Alfred, Florida, as well as an experimental CUPS run by Rhuanito “Johnny” Soranz Ferrarezi, Ph.D., of the University of Florida Institute of Food

and Agricultural Sciences (UF/IFAS) Indian River Research and Education Center in Fort Pierce, Florida. The following day, board members, staff and researchers met with Gary England, director of the UF/IFAS Hastings Agricultural Extension Center in Hastings, Florida, and toured a grove with surviving trees northwest of Orlando.

Presentations indicated that progress made within the research community is promising, but there remain many unanswered questions and no clear path to help the California citrus industry get through this disease unscathed.

Many references were made to the “sleeping dragon” aspect of HLB - the long period of time between infection of a tree with CLas and the appearance of symptoms. The current status of early detection technologies, specifically the lack of validation between indirect, systemic technologies and eventual polymerase chain reaction (PCR)-based confirmation


of disease status remains a challenging limitation to early detection of CLas in California citrus trees. Progress was made with the PCR detection method currently in place with primers of high specificity and sensitivity identified and being tested by regulatory agencies for possible incorporation into regulatory protocols.

New citrus varieties are often viewed as a best-case long-term solution to this disease and with the long development path for new varieties in mind, the CRB partnered with the Citrus Research and Development Foundation (CRDF) of Florida to set up a roundtable discussion bringing together plant breeders (both traditional and molecular) and molecular biologists, as well as other interested parties from all parts of the world for face-to-face introductions, a review of current research efforts to look for prospective collaborations and to review potential stumbling blocks in bringing HLB-resistant citrus varieties to market.

The CRB, along with citrus industry partners, will host the sixth IRCHLB Conference in California in 2019. Stay tuned, as a date and location soon will be announced. Melinda Klein, Ph.D., is the Chief Research Scientist and Carolina Evangelo is the Director of Communications for the Citrus Research Board. For more information, contact [email protected] or [email protected]

CRB President Gary Schulz kicked off the CRB- and CRDF-sponsored Citrus Breeders Roundtable Discussion.


UC Riverside's Citrus DayConnecting Growers and ResearchersCarolina Evangelo

The rain didn’t keep citrus growers or industry members from attending the annual University of California,

Riverside (UCR) Citrus Day on February 7, 2017. The UCR farm shop was jam-packed and saw record-breaking attendance.

The event promoted citrus research activities at UCR and fostered communication between growers and UCR researchers. The one-day experience was filled with speaker presentations that covered topics ranging from Asian citrus psyllid (ACP)/huanglongbing (HLB), preserving citrus for the future and irrigation. About a dozen scientific posters were on display for growers to explore during breaks and lunch

times. A delicious lunch was sponsored by Irrometer and Hortau. The day concluded with an afternoon of field tours and demonstrations.

We want to thank Peggy Mauk, Ph.D., Tracy Kahn, Ph.D., and UCR Ag Operations staff and researchers for coordinating this successful day in cooperation with the Citrus Research Board.

Carolina Evangelo is the CRB director of communications and the co-publisher/project manager of Citrograph. For more information, contact [email protected]

1.) The UCR farm shop was packed with growers and industry members for the day’s talks.

2.) UCR’s Aviva Goldman discussed her poster with CRB Director of Data Management Rick Dunn and UCR student Nichole Ginnan.

3.) CRB Chairman Jim Gorden addressed attendees and delivered a message on behalf of the CRB.

4.)Tracy Kahn, Ph.D., and Peggy Mauk, Ph.D., kicked off the day as Mark Hoddle, Ph.D., looked on.

5.) Toni Seibert, Peggy Mauk, Ph.D., and Karene Trunnelle.

6.) CRB Secretary-Treasurer John Konda, CRB Board Member Greg Galloway and CRB Chairman Jim Gorden.

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HLB in Guangdong, ChinaJianchi Chen

Project SummaryHuanglongbing (HLB or in Chinese, meaning yellow shoot disease) is currently threatening citrus production worldwide. It also is called citrus greening disease in South Africa, emphasizing the improperly colored green fruit on diseased trees. HLB is associated with three uncultivable bacteria: ‘Candidatus Liberibacter asiaticus,’ ‘Ca. Liberibacter africanus’ and ‘Ca. Liberibacter americanus.’ Among them, ‘Ca. Liberibacter asiaticus’ is the most prevalent and the only species found in China, and it also is the only HLB-associated pathogen in the United States. HLB was discovered in Florida in 2005 and in California and Texas in 2012. However, it has been in southern China for more than a hundred years. This article is a brief review of the history and current status of HLB in Guangdong, China, where HLB was first described, and is designed to provide reference information for current efforts in HLB management and research. Guangdong is one of the major citrus-producing provinces in China. Citrus is marketed exclusively for domestic consumption. A number of diverse cultivars are grown, and each cultivar is known to produce the best quality fruit in specific geographical regions. Current citrus production in Guangdong is divided into four regions: east, central, west and north (Figure 1). The east and central regions have a long history of citrus cultivation, while extensive cultivation of citrus in the north and west regions is recent. HLB was observed by citrus growers in the coastal Chaoshan area (east region) in the late 1800s. The first scientific report about citrus “yellowing” disease was made by

O.A. Reinking, Ph.D., in 1919 from his citrus disease survey in the Pearl River Delta area (central region). HLB received little attention until the 1930s, when outbreaks of the disease erupted in the Chaoshan area. In response to the crisis, Chen Che Poh, Ph.D., of the Citrus Experiment Station, Lingnan University/Fukien Provincial College of Agriculture, conducted a four-year survey and research in the outbreak area. He translated HLB as tip-chlorosis in English and noted that nearly all citrus orchards visited were ruined by HLB. Adding to the problem was the unknown cause of the disease. Chen


performed nutrition supplement experiments and concluded that nutrition deficiency was not the cause of HLB. He further monitored the HLB epidemic in orchards, demonstrated the pattern of HLB spread and suggested that a biological factor might be involved in the HLB epidemic (Figure 2). Beginning in the 1930s and extending well into the 1940s, the HLB epidemic subsided, ironically due to citrus acreage reduction during World War II. The war created a demand for more rice production, leading to the conversion of citrus orchards into paddy fields.

From late 1940s into the 1950s, post-war rebuilding led to the rebound of citrus cultivation, apparently without consideration of HLB control. Following the citrus production boom, HLB incidence increased. Again, it quickly became a severe road block in development of the local economy. HLB research was back on the table in the scientific community. The elusive etiology of HLB triggered a heated debate, mainly surrounded by two theories:

HLB was physiological, i.e., caused by nutrient deficiency or, as more scientists came to believe, water logging (note that citrus production in Guangdong by then was mainly in the Pearl River Delta Plain in the central region and Chaoshan or Han River Delta Plain in the east region), or,HLB was pathological, i.e., caused by an infectious disease agent.

The resemblance of HLB symptoms to other physiological disorders and repeated failures to identify a pathogen made the pathological theory unpopular. A milestone was set by Kung-Hsang Lin, Ph.D., at the South China Agricultural College (now South China Agricultural

University), who published a research paper about HLB in Acta Phytopathlogica Sinica in 1956. First, Lin provided detailed descriptions of HLB symptomology. Citrus trees may be affected at any age. Characteristic symptoms were general yellowing of some nearly mature new shoots, dropping of yellow leaves and rotting of rootlets. Pictures of HLB symptoms

Figure 1. Map of Guangdong Province showing the four major regions of citrus production (different shaded levels) with Pefecture-level cities. Mountain ranges are indicated by blue triangles. Both Chaoshan and Pearl River Delta plains with a long history of HLB are highlighted with dotted line ovals. Current major citrus production areas are highlighted by a solid line oval. Picture at the bottom right is the currently popular cultivar, Shatangju, meaning cane sugar mandarin.

Figure 2. A two-year observation of HLB development in an orchard in the Chaoshan area of Guangdong, China, in the 1940s. Explanations in red were added by J. Chen. Note the spread of HLB in the direction of river water flow and the slowing down of HLB when encountering small hills.

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are shown in Figure 3. Nearly all species and varieties of Citrus grown in Guangdong were susceptible. Then, Lin conducted systematically designed experiments to demonstrate that HLB was graft-transmissible, infectious (proposed viral etiology) and likely involved insect transmission. He excluded both physiological disorders (e.g., mineral deficiencies or water

logging) and soil-borne diseases (e.g., nematode or Fusarium infections) as being the cause of HLB.

Based on the “infectious pathogen” theory, three key measures for HLB control were proposed:

use of clean nursery stock with regional quarantine,

removal of diseased trees and insect vector control.

Since Guangdong was in an HLB endemic region, obtaining completely HLB-free nursery stock was challenging at that time. To resolve the problem, Lin initiated research on budwood heat treatment in the 1950s. In 1964, he reported that hot water treatment with temperature ranges inactivating the presumptive HLB-associated pathogen also could kill healthy budwood tissue. However, thermal treatment with water vapor-saturated hot air was effective in killing the presumptive causal HLB agent without affecting budwood viability when grafted onto rootstocks. Temperature range and time lengths are listed in Table 1.

The three key measures worked together effectively under the collective agriculture production system used in China at the time that assured area-wide uniform pest control operations. In the late 1970s, agricultural production in China returned to individual family-run farms, and coordination of pest control became disarrayed as a result. HLB reemerged. Effective control measures were lacking. Citrus production in Guangdong dropped substantially in the 1980s. Starting in the mid-1990s, major citrus production moved to the inland hillock mountainous north and west regions with a highly marketable local mandarin cultivar, Shatangju, meaning cane sugar mandarin (Figures 1 and 4). Acreage quickly reached about 346,000 acres by 2010, but unfortunately, HLB control was ignored again. Infected

nursery stocks spread widely. As a result, HLB began to reemerge, and citrus production in Guangdong is now facing another downward turn. There is currently a high demand for a full understanding of HLB biology so that efficient and effective control strategies can be formulated.

Figure 3. Representative symptoms of HLB in Guangdong, China, in 2010. A: yellow shoots; B: leaf yellowing; C: leaf mottling; D: Zn-deficiency-like.

Figure 4. (A and B) Terraces of Shatangju trees in the hillock and mountainous west region of Guangdong. (C) An HLB-affected tree is shown in the lowland from a distance and (D) a close-up view showing yellow shoots. (E) An orchard with a high incidence of HLB. Photos A-D courtesy of Xiaoling Deng, Ph.D. Photo E courtesy of author.

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The challenge of HLB etiology research was noted in the 1930s in Guangdong by Chen and persisted through the 1990s. Jose Bové, Ph.D., and his group in France identified ‘Candidatus Liberibacter asiaticus,’ an unculturable α-proteobacterium, as the most probable pathogen in 1994. Two years later, the association of CLas with HLB in Guangdong was confirmed by W. Tang, Ph.D., and graduate student X. Deng at South China Agricultural University. Worth mentioning here is that the Asian citrus psyllid (ACP) was confirmed to be the vector of the HLB-associated pathogen in Guangdong in 1977 by researchers at the same university.

While the pathological-based theory of HLB finally prevailed, impacts of physiological factors on citrus health cannot be excluded. However, documentation on the “physiological” etiology of HLB has been rare. There have been occasional legendary stories that HLB symptomatic trees have been cured through improved nutritional management by experienced citrus

growers. These “successes” always have been questioned as to whether “true” HLB-infected trees were encountered, raising the argument of just what is HLB. Impacts of nutrition management on HLB development, particularly at early stages of infection, are very difficult to evaluate due to the woody and perennial nature of citrus and the lack of reliable research tools. There is, however, general agreement that good nutritional management (along with various levels of pest management) on HLB-affected trees can prolong fruit production. This information has been welcomed by growers, particularly when the price of citrus is high.

Today, vigorous research on HLB etiology and

control continues. With the stronger Chinese national economy, several new infrastructure investments have been put in place to resolve the HLB problem. One of them is the Chinese Modern Agricultural Technology Systems, which involves multiple universities and experiment stations in southern China. HLB research is a top priority, receiving stable government support annually. Provincial support for HLB research and control practices also have been established. Because of these government initiatives in HLB research, a research collaboration between the South China Agriculture University and the U.S. Department of Agriculture-Agricultural Research Service at Parlier, California, was established in 2006. One recent contribution, with support from the Citrus Research Board, is the development of a highly sensitive and accurate PCR-based detection system for HLB diagnosis before symptom expression. As molecular and genomic technology become available, we are embracing a new round of research to reveal more details of HLB etiology that

will benefit current HLB management in the U.S., China and around the world.

ReferencesChen C.P. 1943. A report of a study on yellow shoot disease of citrus in Chaoshan. New Agriculture Quarterly Bulletin 3:142-177.

Chen, J.; Deng, X.; Civerolo, E.L.; Lee, R.F.; Jones, J.B.; Zhou, C.; Hartung, J.S.; Manjunath, K.L.; Brlansky, R.H. 2011. ‘Candidatus Liberibacter species,’ without Koch’s postulates completed, can the bacterium be considered as the causal agent of citrus Huanglongbing (yellow shoot disease)? Acta Phytopathologica Sinica 41:113-117.

Deng, X.; Gao, Y.; Chen, J.; Pu, X.; Kong, W.; Li, H. 2012. Current situation of “Candidatus Liberibacter asiaticus” in Guangdong, P. R. China, where citrus Huanglongbing was first described. Journal of Integrative Agriculture 11:424-429.

Lin, K.H. 1956. Research in citrus yellow shoot disease. Acta Phytopathologica Sinica 2:1-42.

Reinking, O. A. 1919. Diseases of economic plants in South China. Philippine Agriculture 8:109-135.

Jianchi Chen, Ph.D. is a research molecular biologist at the USDA-ARS San Joaquin Agricultural Sciences Center, Parlier, California. For more information, contact [email protected]

Temperature (ºC ) Time period46 6 hours48 4, 5 hours 50 1, 1.5, 2 hours 52 30, 45, 60 minutes 54 25, 30 minutes 58 10 minutes 60 2, 3, 5 minutes

Table 1. Temperature and time length of water vapor-saturated hot air treatment of huanglongbing-affected budwood that inactivated the presumptive HLB-associated pathogen determined by grafting experiments.

Note: All time periods listed for a specific temperature were effective. The smallest number was the minimal time to inactivate the HLB pathogen, and the largest number was the maximal time that citrus budwood tolerated and remained viable for grafting.

Source: Lin, K.H.; Zheng, Y. 1964. A preliminary study on the resistance of yellow shoot virus and citrus budwood tissue to heat. Acta Phytopathologica Sinica 7:61-65


Figure 1. Fruit scarring on navel oranges caused by citrus thrips. A rating scale of 0-4 was used with (A) slight scarring category 1 is any minor scar, (B) category 2 is a light or partial ring, (C) severe

category 3 is a complete ring or heavy partial ring and (D) category 4 is a heavy scar.

A

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Joseph G. Morse and Elizabeth E. Grafton-Cardwell

Do Broad-spectrum Pesticides Induce Citrus Thrips Damage?Project SummaryFor many years, pesticide efficacy trials were run with citrus thrips at the Lindcove Research and Extension Center (LREC) near Exeter, California. Citrus thrips fruit scarring data are presented for 33 years on trees that were left as untreated controls in these trials and show that scarring varied a great deal from year to year. We present the hypothesis that citrus thrips is often a pesticide-induced pest and that when selective pesticides are used for control of it and other citrus pests,

CRB-FUNDED FINAL RESEARCH REPORT


citrus thrips fruit scarring is greatly reduced. As we deal with huanglongbing (HLB) more in California, greater use of broad-spectrum materials will be needed for control of Asian citrus psyllid (ACP), and citrus thrips is likely to re-emerge as a greater problem, similar to what was seen during the organophosphate/carbamate era in California.

Citrus thrips, Scirtothrips citri, first described in 1907 by USDA scientist Dudley Moulton, has long been known as a California citrus pest. Citrus thrips are native to the southwestern U.S. and northwestern Mexico. Prior to the introduction of citrus to the region, it was common on host plants such as laurel sumac (Malosma laurina) and several live oak species (Quercus spp.) (Morse 1995).

Between 1972–81, Bill Ewart, Ph.D., and/or O.L. Brawner ran citrus thrips pesticide efficacy trials in Field 12 (Atwood navel oranges) at the LREC. After Ewart retired, Brawner continued these trials, and between 1983 and 2004, Joseph Morse, Ph.D., and Brawner/Alan Urena continued these studies using similar methods. Each year, the four-acre field was divided into four-tree plots (two trees per row in two adjacent rows, forming a square). Four or more plots (minimum of 16 trees) were randomly selected to serve as untreated controls. In October, all outside fruit (1.5 feet or less inside the tree) from knee to eye level were rated for scarring caused by citrus thrips using a standard 0-4 rating scale (0, no thrips scarring; 1-2 slight; 3-4 severe = economic fruit scarring; [Figure 1]; see Grafton-Cardwell et al. 2003, Morse et al. 2016).

During the first 26 years of the study (1972-97), average percentage severe scarring caused by citrus thrips was 24.9 percent (ranged from one percent in 1995 to 69 percent in 1988); Figure 2. In eight years, severe scarring was less than ten percent and in only three was it less than five. In 10 of the 26 years, severe fruit scarring was more than 25 percent (mean of 49.9 percent).

In contrast, between 1998 and 2004, the percentage severe fruit scarring averaged 0.6 percent, ranging from 0.1 percent (2000) to 1.2 percent (1999). A second observation over these latter years was that the level of citrus thrips fruit scarring on untreated control trees often was less than that in plots with many pesticide treatments – in particular, those that were not highly effective against citrus thrips based on weekly counts of immature thrips levels on fruit.

Obviously, something changed between these two time periods. After seven years (1998-

Figure 2. Historical data for slight and severe (economic) fruit scarring on Atwood navel orange trees in Field 12 at the LREC (2004 data from Field 41-42).

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Fig. 4. Historical Citrus Thrips Fruit Scarring on Untreated Trees in Field 12 at LREC

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2004) of conducting pesticide efficacy trials and obtaining little useful data due to low levels of scarring on untreated control trees, we discontinued field citrus thrips trials at Lindcove in 2005 and instead conducted pesticide screening trials on laurel sumac bushes in Riverside greenhouses.

Between 1972-1997, organophosphates (OPs), carbamates and pyrethroids were the primary materials used at Lindcove and in the vicinity to control citrus thrips, California red scale and katydids or orangeworms. All three of these classes of chemistry are relatively broad-spectrum in their activity (they impact a wide range of pests and natural enemies), and they are also relatively persistent on leaf and fruit surfaces. Once Success® was registered in 1998, most growers started using that material heavily for citrus thrips control, but continued pyrethroid and OPs use for katydid control (Figure 3). Delegate® is similar in chemistry to Success. It was registered in 2007 and became the citrus thrips insecticide of choice due to its greater

efficacy and persistence. In 2011 (Morse and Grafton-Cardwell 2012), we began to see the beginnings of citrus thrips resistance to Success/Delegate; but so far, this has been seen only on a limited basis in groves where past use has been high. Success, Agri-Mek®, and Delegate are relatively selective pesticides. All three materials are broken down by sunlight (Success>Agri-Mek>Delegate) and show translaminar movement, i.e., they move into the upper cell layers of leaves and fruit, in particular with the addition of a small amount of oil. However, leaf feeders such as citrus thrips, orangeworms and ACP (with Success and, in particular, Delegate, which is also more persistent) or citrus thrips and mites (Agri-Mek) continue to be killed after surface residues have declined to sub-lethal levels.

The pattern of pesticide use for California red scale (Figure 4) followed a similar pattern as that seen with citrus thrips. From the 1970s until 1998, organophosphates (Supracide®, Lorsban® and, to a lesser extent, malathion and the carbamate Sevin®) were the main materials used for control, but red scale resistance to these materials started to appear in the mid-1990s. Resistance required multiple scale treatments per year and led to emergency registrations allowing the use of two insect growth regulators (IGRs), Esteem® and Applaud® in 1998 and 1999, respectively. The two IGRs are relatively selective pesticides.

We believe this shift in chemistry used for control of citrus thrips and California red scale away from organophosphate and carbamate insecticides is largely responsible for citrus thrips becoming a less severe pest starting in 1998 or perhaps a bit earlier. In part, lesser

severity of citrus thrips could be due to greater control by natural enemies such as spiders, predaceous thrips, lacewings, predaceous mites and others, which were impacted to a lesser degree by the more selective materials used for citrus thrips and California red scale control.

However, we hypothesize that stimulation of citrus thrips (hormoligosis, the popular term in entomology literature, or hormesis, the more common term in medical literature) is probably an even more important factor in the observed reduced severity of citrus thrips starting in the late 1990s. Hormoligosis/hormesis is a biological phenomenon whereby a beneficial effect (improved health, stress tolerance, growth, longevity or fecundity) results from exposures to low doses of an agent that is otherwise toxic or lethal when given at higher doses (Luckey 1968; Calabrese 2005; Mattson 2008). We first suspected that marginally effective pesticides might stimulate citrus thrips when we often saw higher levels of fruit

Figure 3. Insecticides used for citrus thrips and katydid control in the San Joaquin Valley. It is difficult to separate which insect the pesticide is used for; treatments for thrips and/or katydids are often tank mixed.

Figure 4. Insecticides used for California red scale control in the San Joaquin Valley.

050,000

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Fig.2.InsecticidesUsedforCitrusThrips &KatydidControlintheSanJoaquinValley

dimethoate Carzol Baythroid DanitolAgri-Mek Veratran Success Delegate

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Fig. 3. Insecticides Used for California Red Scale Controlin the San Joaquin Valley

Sevin Supracide Lorsban Esteem Applaud Movento


scarring with various insecticides in Field 12 pesticide efficacy trials compared to untreated control trees. To evaluate this, we exposed citrus thrips females to sub-lethal rates (rates expected to cause 0.01, 0.1, 1, and 10 percent mortality based on previous testing of each material) of four pesticides (the pyrethroid Mavrik®, carbamate Carzol®, organochlorine Kelthane® and organophosphate malathion) over a 48-hour period and observed how many offspring were produced. With each of the four materials evaluated, at least one of the tested rates (0.01 percent mortality three times, 0.1 percent once, 1 percent once) resulted in statistically higher citrus thrips offspring production than was seen on untreated control leaves (Morse and Zareh 1991).

Entomology literature contains a large number of references to “mite resurgence” following insecticide or miticide treatments. However, it was not until one of us was approached to provide an article for the BELLE (Biological Effects of Low Level Exposures) Newsletter (Morse 1998) that we realized that hormoligosis is well recognized by doctors, toxicologists and pharmacologists as a widespread biological phenomenon (Calabrese 2009, other BELLE Newsletters, http://www.belleonline.com/newsletters.htm, published between 1992-2010).

In recent years, citrus thrips populations also have been aggravated by heat and drought that accelerate thrips development and increase their survival, in particular, pupal stages in the soil (Schweizer and Morse 1997a, b). Thus, a number of factors including pesticide resistance, drought and hormoligosis can create a “perfect storm” that makes citrus thrips management difficult.

We expect that once HLB is detected in California commercial citrus groves, treatments for control of ACP will necessarily increase in frequency with at least some treatments utilizing broad-spectrum pesticides. Florida growers have reported that mite, scales and other secondary pests have become more severe with added ACP treatments in that state. Unfortunately, we believe citrus thrips again will become a more severe pest once we need to control ACP to a greater degree. We see little that can be done to avoid this. We believe one of our biggest pest management challenges will be to rotate the chemistries we have available for various pest species such as ACP, citrus thrips and California red scale so as to slow the rate at which effective materials are lost to pesticide resistance. We likely will have to live with hormoligosis/pest resurgence until longer-term non-chemical solutions to the HLB crisis are developed.

CRB Research Project #5500-501b

AcknowledgementsThis research was supported in part by grants from the Citrus Research Board. We thank O.L. Brawner, Alan Urena and Pamela Watkins for technical assistance and the LREC staff for their assistance in running trials at the Lindcove Field Station.

ReferencesCalabrese, E.J. 2005. Cancer biology and hormesis: human tumor cell lines commonly display hormetic (biphasic) dose responses. Critical Reviews in Toxicology 35:463-582.

©2016 Nichino America, Inc. All rights reserved. Centaur and Nichino America logo are registered trademarks of Nichino America, Inc. Always read and follow all label directions. Refer to global MRL database for current established tolerances: www.globalmrl.com/db#query 888-740-7700 | www.nichino.net

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Calabrese, E.J. 2009. BELLE: an evolving legacy. A brief history of BELLE: Introduction. BELLE Newsletter 15(2):1-2.

Grafton-Cardwell, E.E.; O’Connell, N.V.; Kallsen, C.E.; Morse, J.G. 2003. Photographic guide to citrus fruit scarring. University of California Division of Agriculture and Natural Resources Publication 8090, Oakland, California. 8 pp.

Luckey, T.D. 1968. Insecticide hormoligosis. Journal of Economic Entomology 61(1):7-12.

Mattson, M.P. 2008. Hormesis defined. Ageing Research Review 7(1):1-7.

Morse, J.G. 1998. Agricultural implications of pesticide-induced hormesis of insects and mites. Human & Experimental Toxicology 17(5):266-269.

Morse, J.G. 1995. Prospects for IPM of citrus thrips in California. In: B.L. Parker, M. Skinner and T. Lewis (eds.), Thrips Biology and Management 276:371-379. NATO ASI Series, Springer-Verlag, USA.

Morse, J.G.; Grafton-Cardwell, B. 2012. Management of citrus thrips to reduce the evolution of resistance. Citrograph 3(2):22-30.

Morse, J.G.; Zareh, N. 1991. Pesticide-induced hormoligosis of citrus thrips (Thysanoptera: Thripidae) fecundity. Journal of Economic Entomology 84(4):1169-1174.

Morse, J.G.; Urena, A.A.; Robinson, L.J.; Watkins, P.J. 2016. Citrus thrips fruit scarring: differing susceptibility of citrus varieties. Citrograph 7(3):44-47.

Moulton, D. 1907. A contribution to our knowledge of the Thysanoptera of California. USDA Bureau of Entomology Technical Series Bulletin 12, Pt. III. 39-68 pp.

Schweizer, H.; Morse, J.G. 1997a. Factors influencing survival of citrus thrips (Thysanoptera: Thripidae) propupae and pupae on the ground. Journal of Economic Entomology 90(2):435-443.

Schweizer, H.; Morse, J.G. 1997b. Estimating the level of fruit scarring by citrus thrips from temperature conditions prior to the end of bloom. Crop Protection 16(8):743-752.

Joseph G. Morse, Ph.D., is a professor of entomology at the University of California, Riverside, and Elizabeth E. Grafton-Cardwell, Ph.D., is an extension specialist at the University of California, Riverside and also director of the Lindcove Research and Extension Center. For more information about this report, contact [email protected] D D E S I G N ( P R O O F )

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Timing of Adult Fuller Rose Beetle Soil Emergence Joseph G. Morse, Phil A. Phillips, Donald L. Flaherty, Neil V. O’Connell, Peter B. Goodell, Anthony A. Urena and Elizabeth E. Grafton-Cardwell

Project SummaryIn recent years, the Fuller rose beetle (FRB) has become problematic for California export shipments to South Korea. For growers to optimally time management strategies such as skirt-pruning, ground sprays and/or foliar sprays, it is important to understand the phenology¹ of adult beetle emergence out of the soil. The following data were collected during 1986-1989 after FRB became an export issue for California citrus sent to Japan. The first year of data were previously reported by Morse et al. (1987), but now that the beetle has re-arisen as an export concern, we are summarizing the full three-year data set below and discussing how the timing of soil emergence varies somewhat in the three areas of California where research was conducted.

CRB-FUNDED RESEARCH PROGRESS REPORT

Figure 1. Fuller rose beetle egg masses under the button of the citrus fruit stem end.

UC Statewide IPM Project© 2000 Regents, University of California


The Fuller rose beetle, Naupactus godmani (Crotch), goes by a number of different Latin (Asynonychus cervinus, Naupactus cervinus, Pantomorus olindae, Aramigus fulleri and others) and common names (such as Fuller rose weevil) in the scientific literature. In California citrus, it is seldom considered a pest, other than when it interferes with shipment of fruit to countries where it is a quarantine pest. Also, it is occasionally problematic when feeding on isolated replants in a grove or on the small buds of top-worked citrus when top-working coincides with a large emergence of adults out of the soil.

This insect typically has one generation per year and spends most of the year underground as a larva feeding on the roots of citrus and a few other host plants such as blackberries, cherries, raspberries, roses and strawberries. The beetle is flightless, and thus, skirt-pruning and trunk-banding (although laborious and expensive) are two methods of preventing beetle access to leaves to feed on, which is required before eggs are produced. It is also parthenogenetic2 (females only). After feeding for a week or two on the leaves of a number of host plants including citrus, it will lay eggs in cracks or crevices in the tree or under the sepals of citrus. Ninety-five percent egg hatch occurs after 557.6 degree-days above a 51°F threshold (309.8 above 10.6°C; Morse and Lakin 1987), and neonate larvae hatch and drop into the soil to find roots on which to feed. Larvae feed for six to ten months, pupate in the soil; then adults emerge out of the soil and climb trees.

Until about 1985, FRB was a well known, but ignored, minor pest of California citrus. Then Japanese inspectors detected FRB eggs under the button of the citrus fruit stem end

(Figure 1) shipped from the U.S. and Australia and started fumigating contaminated loads with methyl bromide, which was both damaging to the fruit and costly to growers. In 2005, following a World Trade Organization (WTO) challenge, FRB was deleted from the list of actionable pests in Japan after its discovery in a Japanese citrus grove. Fuller rose beetle re-arose as a pest of concern in 2011, and is currently listed as an actionable, quarantine pest by South Korea.

FRB management is problematic, partly because it is often unknown in advance which groves will be harvested for export to countries where FRB is of concern. Control is costly, and packinghouses so far have been unwilling to provide a premium to growers who manage FRB effectively, suggesting instead that all growers should maintain low populations. California citrus is grown in four climatically divergent growing regions – the southern California desert area in the Coachella Valley, interior southern California, coastal southern California and the San Joaquin Valley. Fuller rose beetle populations appear to be highest in interior and coastal southern California, sporadic in the San Joaquin Valley and lowest in the Coachella Valley. The aims of the following study were to determine the months of the year and relative levels of adult FRB soil emergence in each of the three California citrus growing regions, exclusive of the Coachella Valley.

Adult FRB soil emergence was monitored by selecting citrus groves with known high populations, searching for trees with signs of heavy past adult feeding activity on interior leaves (Figure 2), and placing emergence boxes near the water emitter where roots were likely to be present and would catch

Figure 2. Leaf feeding damage by FRB adults.

UC Statewide IPM Project© 2000 Regents, University of California


emerging adults (Figure 3). Sampling was initiated in July or August 1986 in 13 groves, and the study was run over a three-year period at ten sites, or over a two-year period at two sites (McFarland and Ojai). Due to low emergence, two groves were dropped from sampling after the first year (data not shown), and a new grove (Ojai) was added in August 1987, resulting in

a total of four groves in each region (Table 1). Emergence boxes were two-feet square, built of 2” x 6” high wood frames, and were covered on top with wire screening. The box was worked into the soil to a depth of 0.5 inches so that adults could not escape and was checked every one to two weeks for emergence by counting and removing all adults, which were placed outside the box to allow them access to the tree. Adult FRB “play dead” when disturbed, so shaking the box as it was removed from the soil resulted in them dropping to the soil surface where they could be counted easily.

Emergence data (Figure 4, Table 2) show that FRB adults emerge out of the soil every month of the year, but the majority of emergence occurs June through November, with some differences between regions. In the four interior southern California groves (Figure 4a), soil emergence was low in June,

increased in July, was heaviest over the three months of August through October, decreased slightly in November, more so in December and was quite low from January through May. In the three coastal groves (Figure 4b), emergence started a month earlier, increased in June, was highest for the three months of July through September, but tailed off more slowly (95 percent of the annual emergence occurred over the six months of June through November). Emergence in the four San Joaquin Valley (SJV) groves (Figure 4c) was more tightly clumped, with July through September again being the three high months, and 83.5 percent of the annual emergence occurring during those three months.

The moderately high emergence during January through March in the SJV was a bit odd. Based on the data broken down by grove for this time period (Figure 4c), the McFarland grove had one percent of the annual emergence in January, Strathmore 1.7 and 3.6 percent in February and March, and Lindsay 8.4 and 3.9 percent in January and February. In particular, we discount the Lindsay January data, as there were only 20 traps at this site. Emergence levels at this grove were relatively low (3.2 beetles per trap during the entire year; mean of 10.2 for the other three SJV sites; mean of 12.0 at the eight sites in southern California). This higher winter emergence did not occur consistently each year.

0

1

2

3

4

5

6

7

8

9

10

11

12

Jul-86 Oct-86 Jan-87 Apr-87 Jul-87 Oct-87 Jan-88 Apr-88 Jul-88 Oct-88 Jan-89 Apr-89

Bee

tles/

Tra

p/ /M

onth

Month-Year

Fig. 4a. Riverside / SB Counties

Hemet-Valencia

Hemet-Grapefruit

Corona-Grapefruit

Redlands-Grapefruit

0

1

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3

4

5

6

7

8

9

10

11

12


Bee

tles

/ Tra

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onth

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Fig. 4c. Tulare / Kern Counties

McFarland-Navel

Strathmore-Navel

Ivanhoe-Navel

Lindsay-Valencia

0

1

2

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4

5

6

7

8

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/ Tra

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Fig. 4b. Ventura County Somis-Valencia Fillmore-Lemon Fillmore2-Lemon Ojai-Valencia

Fig. 3. Fuller rose beetle adult.

Fig. 4. Number of adult Fuller rose beetles emerging per trap per month at each of the 12 monitoring sites. To keep graphs on the same y-axis scale, datum for the McFarland site during August 1986 is not shown (Figure 4c; 18.59 beetles emerged per trap for that month).


File = Tables 1, 2_Orignial-v2.xls; Date Printed = 4/28/17; Page = 1

Table 1. Fuller rose beetle soil emergence site location data.

Site # Nearest City County # of trapsStart-End of

SamplingScion Rootstock Planting Date Soil Type

1 Hemet Riverside 40 7/86 - 9/89 aOld Line Valencia

Carrizo citrange 1930Romona sandy loam in association with Hanford fine and coarse sandy

loam

2 Hemet Riverside 40 7/86 - 8/89 aMarsh

grapefruitTroyer citrange 1981 See 1 above

3 Corona Riverside 40 7/86 - 9/89Red Blush grapefruit

Swingle citrumelo

1961Garretson gravelly very fine loam in

association with Cortina cobbly loam and Arbuckle gravelly loam

4 RedlandsSan

Bernardino40 7/86 - 8/89

Marsh grapefruit

Swingle citrumelo

1960Hanford sandy loam with Tujunga loamy sand and Tujunga gravelly

loamy sand

5 McFarland Kern 40 8/86 - 3/88Troyer navel

Nucellar navel 1968 Chanac clay loam

6 Strathmore Tulare 20 8/86 - 3/89Old Line

navelTroyer 1965 Exeter loam and Honcut sandy loam

7 Ivanhoe Tulare 20 8/86 - 3/89Old Line

navelTroyer 1963 San Joaquin sandy loam

8 Lindsay Tulare 20 8/86 - 3/89Old Line Valencia

Sour orange 1935 Exeter loam

9 Somis Ventura 20 7/86 - 3/89Old Line Valencia

Campbell Valencia orange

1961Sorrento silty clay loam in the

Mocho-Sorrento-Garretson Association

10 Fillmore Ventura 20 7/86 - 3/89Monroe lemon

Limco 8A lemon 1966

Mocho loam (deep, poorly drained loamy sand to silty clay loam in the

Mocho-Sorrento-Garretson Association)

11 Fillmore2 Ventura 20 7/86 - 3/89Eureka lemon

Macrophylla lemon

1974 See 10 above

12 Ojai Ventura 20 5/87 - 3/89Old Line Valencia

Sweet orange 1935Garreston gravally loam in the Pico-Metz-Anacapa Association (sandy

loams generally)

a Sites 1 and 2 had missing data for April and May 1988.Table 2. Phenology of Fuller rose beetle soil emergence in 3 citrus growing regions in California (months with > 5%

are in bold text).

Percent of yearly emergence per month (mean for four groves per region over two to three years per grove)

Region Jan. Feb. Mar. Apr. May June July Aug. Sept. Oct. Nov. Dec.Peak 3

months% over

peak 3 mo.

Interior southern Calif. 0.25% 0.13% 0.14% 0.00% 0.03% 1.37% 7.34% 23.08% 28.62% 25.98% 11.00% 2.07% Aug.-Oct. 77.7%

Coastal southern Calif. 1.13% 0.19% 0.17% 0.08% 1.41% 12.38% 19.97% 28.09% 17.64% 11.75% 5.17% 2.03%July-Sept.

65.7%

San Joaquin Valley 2.56% 1.48% 1.19% 0.09% 0.03% 5.45% 19.60% 40.33% 23.52% 3.86% 1.50% 0.39%July-Sept.

83.5%

Table 1. Fuller rose beetle soil emergence site location data.

Table 2. Phenology of Fuller rose beetle soil emergence in three citrus growing regions in California (months with more than five percent are in bold text).

aSites 1 and 2 had missing data for April and May 1988.

In using these emergence data to time FRB management strategies, we suggest that skirt-pruning be done in June in interior southern California and in May in the coastal region and SJV. So that the weight of maturing fruit does not bend the skirt down to the ground and allow a bridge for FRB adults into the tree, pruning should be done to a height of 1.5-2 feet (46-61 cm)

off the ground. A small amount of fruit production is lost the first year after pruning, but the tree easily compensates for this over time, resulting in little change in production after two to three years and with the touch-up pruning needed to maintain high skirts. If soil or trunk sprays are used, these might go on early July in interior southern California, and early June in the other two


regions. The purpose of soil treatments is to cause mortality of adults as they emerge from the soil, thus sprays going on too late are ineffective once the beetles are already up in the tree. Foliar sprays are applied during and after the period of peak emergence and are designed to prevent adults that have reached the fruit from laying eggs that would be viable at harvest.

See the UCIPM Guidelines for Citrus for more information on treatments (http://ipm.ucanr.edu/PMG/r107300311.html). Complete control of FRB in the orchard is difficult because adults can emerge at any time of year, and it is difficult to keep the trees protected for long periods. The best long-term solution to the FRB situation would be a post-harvest treatment of only those fruit being exported to a country with quarantine concerns. Research is underway to identify effective treatments that can be used post-harvest.

CRB Research Project #5500-501 (CRB grants from 1985-1989 funded collection of soil emergence data)

Glossary¹Phenology: The relationships of insects’ life cycle stages to environmental factors (i.e., seasonal changes, weather, climate, etc.).

2Parthenogenetic: Ability of some female insects and flowers to reproduce, even if males are absent.

AcknowledgementsThis research was supported in part by grants from the Citrus Research Board. We thank Pamela Watkins for technical assistance and Corona Foothill Citrus, John Gless, Harry Griffiths (deceased), Bob Haury, Ed Lorenzi (Sun Pacific Farming), and Washburn and Sons Citrus Pest Control for allowing us to perform research in their

citrus groves. We also thank Andrew Cline, Ph.D., CDFA Plant Pest Diagnostic Center, for information regarding FRB taxonomy and larval host range.

ReferencesGriffiths, H.; Hardison, A.; Morse, J.G.; Luck, R.F. 1986. Fuller rose beetle: a practical solution. Citrograph 71:139-140.

Lakin, K.R. and J.G. Morse. 1989. A degree-day model for Fuller rose beetle, Pantomorus cervinus (Boheman) (Col., Curculionidae) egg hatch. Journal of Applied Entomology 107:102-106.

Morse, J.G.; Grafton-Cardwell, E.E. 2013. Bifenthrin trunk sprays as a strategy for Fuller rose beetle (FRB) field control in 2013. Citrograph 4(2):26-33.

Morse, J.G.; Phillips, P.A.; Goodell, P.B.; Flaherty, D.L.; Adams, C.J.; Frommer, S.I. 1987. Monitoring Fuller rose beetle populations in citrus groves and egg mass levels on fruit. Pest Control Circular 547:1-8, Sunkist Growers, Inc.

Morse, J.G.; Lakin, K.R. 1987. A degree-day model for Fuller rose beetle. Citrograph 72:O-P.

Joseph G. Morse, Ph.D., is a professor of entomology at the University of California, Riverside; Phil A. Phillips, Ph.D., is a retired IPM advisor in Ventura County; Donald L. Flaherty and Neil V. O’Connell are retired cooperative extension advisors, Tulare County; Peter B. Goodell, Ph.D., is an IPM advisor at the Kearney Agricultural Research and Extension Center; Anthony A. Urena is a retired staff research associate at the University of California, Riverside who worked for many years in the Morse lab; and Elizabeth E. Grafton-Cardwell, Ph.D., is an extension specialist at the University of California, Riverside and director of the Lindcove Research and Extension Center. For more information about this report, contact [email protected]

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CRB-FUNDED FINAL RESEARCH REPORT

Detectation of 'Candidatus Liberibacter' Infection in California CitrusDarya Mishchuk, Xuan He and Carolyn Slupsky

Project SummaryThe California citrus industry is in urgent need of a precise, high-throughput and systematic detection strategy that will prevent ‘Candidatus Liberibacter asiaticus’ (CLas, the pathogen) from spreading and eventually eliminate huanglongbing (HLB). The only currently accepted diagnostic test by the US Department of Agriculture (USDA) Animal and Plant Health Inspection Service (APHIS) uses polymerase chain reaction (PCR) technology to detect the DNA of the pathogen that is associated with HLB. PCR assays may not identify trees that are infected. In 2011, our lab began development of a novel and potentially more accurate detection method for HLB that involves measuring plant response to CLas infection reflected as changes in leaf metabolite concentrations. The purpose of this project was to begin optimization of our method for high throughput screening, and to survey California for this disease. This project was done in collaboration with the California Department of Food and Agriculture (CDFA), and the Citrus Research Board (CRB).


HLB in CaliforniaHLB is a devastating citrus disease that is threatening the citrus industry worldwide. The agent associated with this disease, CLas, is spread from tree to tree by the insect Diaphorina citri, or the Asian citrus psyllid (ACP). HLB is widespread in Florida and Texas, and the effect of this disease on citrus fruit production is disturbing. Virtually all citrus groves in Florida have some level of HLB infection, and significant reductions in citrus fruit yields are evident (Grafton-Cardwell et al. 2016). In 2015, it was reported that approximately 80 percent of commercial citrus in Florida was infected, with 15 percent of groves having 100 percent infection, resulting in a 42 percent reduction in yield in 2014 compared with the 2004-2005 harvest (http://edis.ifas.ufl.edu/fe983).

In California, the first tree with HLB was found in March 2012 in a residential area of Hacienda Heights in Los Angeles County (Kumagai et al 2013). In 2015, 10 additional HLB-positive trees and four positive ACP samples were found in San Gabriel about 15 miles north of Hacienda Heights (Hornbaker and Kumagai 2016). Now, more than 40 trees have tested positive for CLas in the Los Angeles Basin (http://citrusinsider.org/2017/03/hlb-detected-again-in-san-gabriel/#more-2691), suggesting that the disease is progressing and could be more widespread. Given that the latest quarantine map for HLB includes 275 square miles in the Los Angeles area as of January 23, 2017, (https://www.cdfa.ca.gov/plant/PE/InteriorExclusion/hlb_quarantine.html), and for ACP, nearly 62,743 square miles of Southern, Central and Northern California (https://www.cdfa.ca.gov/plant/acp/regulation.html), it is very likely that there are more infected trees that have not been identified. With no cure available, to prevent an epidemic and keep citrus production maximal, commitment to the identification and removal of infected trees and controlling ACP populations is needed by growers and the public if we are to continue to produce and consume fresh citrus grown in California.

The PCR-based method: the traditional, direct CLas detection methodDirect detection technologies identify the presumptive pathogen itself (Li et al. 2006). In the case of the PCR-based method, detection is through measurement of pathogen-specific DNA. However, this method is not perfect. First, the number of CLas bacteria in the sample must exceed a certain threshold. This is a tough requirement because it becomes a sampling issue. CLas is not evenly distributed within a tree, and, therefore, random leaf samples collected from an infected tree may not have any or enough bacteria present to allow detection. Another challenge of the PCR-based method is the specificity of the primers. Because PCR-based methods target a region of the bacterial genome, when a DNA primer sequence is not specific enough, DNA belonging to other unrelated bacteria may be falsely detected, resulting in a false

positive. For this reason, true positives are always confirmed through sequencing. Thus, the low sensitivity of the PCR-based method suggests that field validation experiments are challenging, since if the insect vector is present, disease status is unknown.

Metabolomics-based detection: the new innovation based upon plant pathogen defense Metabolism in an organism is driven by proteins/peptides and small molecular weight chemicals called metabolites. These molecules are dynamic, changing in activity and amount to meet the energy demands of the organism and ensure survival. Once infected with a pathogen, plants immediately begin to defend themselves, and an organism’s metabolism is ramped up to defend against the pathogen. This metabolism is very different from when the organism is not infected, or when an organism is exposed to a stressor, such as low nutrient availability. Before symptoms of HLB appear, CLas infection causes a defense response that spreads throughout the plant, changing the tree’s metabolic profile. The pattern of these metabolites during CLas infection defines the “CLas-infected” metabolite profile. Thus, comparison of an unknown metabolite profile to known profiles of infected and non-infected leaf material using a computer-based algorithm allows for prediction of infection status. The beauty of this method is that only a single leaf per tree potentially needs to be sampled, and it does not require selecting for a leaf that “looks infected” (almost any healthy-looking leaf can be used). This sort of measurement is a potentially indirect method of detection of HLB-infected trees, since it detects the response to infection rather than the pathogen itself (Slupsky et al. 2013, Chin et al. 2014, Chin et al. 2015).

Our greenhouse work (manuscript submitted for peer-review) indicated that our metabolomics-based technique can presumptively identify infected trees well before visible symptoms and sooner than PCR-based methods. Field validation of our method in the Texas 2 experiment revealed nearly 100 percent sensitivity and specificity with several trees originally of unknown status and deemed negative by PCR-based methods identified as presumptively positive by our method. This has since been confirmed by PCR (McRoberts, personal communication). In this CRB-funded project, application of our model to classify selected samples from California produced robust results with all samples collected from infected trees in San Gabriel correlating perfectly with qPCR results as positive for CLas, and samples known to be negative for CLas (that included samples with other citrus diseases) correlating with our known CLas negative class. Validation studies to further refine our classifiers to ensure other conditions do not confound our results are continuing, with new field samples being received continually.


Optimization and why automation is a must for our techniqueSince the beginning of the project, 1,014 out of 3,116 samples from urban and commercial growing areas (provided by the CDFA, CRB and citrus growers in Southern, Central and Northern California) were processed and analyzed. Most of these samples were collected by the CDFA between 2013 and 2015 in Hacienda Heights around the initial HLB find encompassing three zones from a 400-meter to a 1,200-meter radius. If funded for high throughput development, we will analyze the remaining 2,102 samples.

Handling of this large volume of samples and data required us to develop a system to allow easy storage and retrieval of sample information (e.g. coordinates, variety, handling information, etc.), and thus a database structure was built (Figure 1). This database contained sample metadata collected from the field (collection date, GPS coordinates, ACP counts, condition of the tree, etc.), and sample tracking within the lab (receipt date, condition of sample, sample preparation, data acquisition, data analysis). Since the metadata were not collected in a consistent manner, we also designed a pattern-matching feature that allowed information to be searched,

combined and stored in a consistent format. If we are able to continue development of our method, the work accomplished here will help us quickly set up a system to track samples and ensure robust data handling.

We also refined our sample preparation protocol so it could be easily used with a liquid handler (a robot system) for high-throughput, automated analysis. Our initial extraction method was based upon a chloroform/methanol method, which was not suitable for high throughput screening due to the volatility and toxicity of these chemicals. We subsequently developed an extraction method using a buffer-based system that produced similar results in approximately one-fifth of the time and at a fraction of the cost (Figure 2).

Still, with this new protocol, we were only able to process and analyze about one-third of the samples received.

A key bottleneck in our process is computer-automated analyses of our data (Figure 2). Currently, well-trained experts must perform analyses manually. To overcome this challenge, toward the end of the funding period, our research team began a significant effort to automate our method; however, additional funds are required to complete software development. Nonetheless, this project has set the foundation for future large-scale screening of citrus samples. If we are successful at securing additional funding for software development, we will be able to scale analysis to 4,000 samples/month on a single instrument.

Importance for California citrus growersSince there is no cure for HLB, finding ways to control its spread is the only way to maintain citrus production in California. The traditional PCR-based screening test for HLB is not perfect. While we have developed a more sensitive metabolomics-based screening test that allows for the presumptive detection of plant host responses to infection prior to the development of disease symptoms, at the current stage, it is limited by its low throughput. Once the automation pipeline

Field DataAddress, GPS coordinates, citrus

variety, collection date, ACP numbers, notes, etc.

Sample HandlingReceipt date, condition of

sample, sample preparation, data acquisition, data analysis

Searchable databaseKeep track of each sample from the moment it is collected until

�nal results

Unique sample identifier

Partial pattern matching

ResultsPredicted HLB infection

status

Step 1Simpli�ed sample processing. Extraction

adapted to automatic liquids handler.

Step 2Automated NMR data acquisition

(already available)

Step 3Metabolite identi�cation and

quantitation, and statistical analysis.

Figure 1. System for entry, archiving and retrieval of sample information. Field metadata is highly variable and dependent on the surveyor collecting it. The system is able to parse these data using a partial pattern-matching algorithm, after which it is combined with sample data collected in the lab. This allows the final result to be easily searchable based on any variable the user chooses to investigate.


is fully developed and validated, we anticipate that growers and government agencies can take advantage of our new HLB detection method to screen and identify trees suspected of being infected that can then be targeted for confirmation by PCR-based methods or removed. This work will also be potentially important for monitoring incidence and spread of HLB throughout California.

CRB Research Project #5300-162

AcknowlegementsThe authors would like to thank Victoria Hornbaker, Lucita Kumagai and MaryLou Polek, Ph.D, for critical reading of the article; Emily Padhi and Rachel Lombardi for help with Figure 2; as well as Laurynne Coates, Elizabeth Chin, Rebecca Lobo, Ann Spevacek and undergraduate students in the Slupsky lab for technical assistance. This project was supported by funding from the Citrus Research Board. Additional support was provided by USDA National Institute of Food and Agriculture Hatch Project 1005945.

ReferencesChin, E.; Lobo, R.; da Graça, J.; Hilf, M.; McCollum, G.; LeVesque, C.; Godfrey, K.; Slupsky, C. (2015) Early detection of HLB with metabolomics. Citrograph 6(2):32–34.

Chin, E.; Mishchuk, D.O.; Bruce, J.; Cilia, M.; Coaker, G.; Davis, C.; Jin, H.; Ma, W.; Sellar, G.; LeVesque, C.; Godfrey, K.; Slupsky, C.M. (2014) An interdisciplinary approach to combat HLB: research in UC Davis’ Contained Research Facility. Citrograph 5(1):28–34.

Grafton-Cardwell, B.; Irey, M.; Bartels, D.; Slupsky, C.; McRoberts, N. (2016) Immediate action is needed: summary of the HLB Summit Morning Session. Citrograph 7(2):24–26.

Hornbaker, V.; Kumagai, L. (2016) HLB Detection in San Gabriel: where we are now? Citrograph 7(1):24–27.

Kumagai, L.B.; LeVesque, C.S.; Blomquist, C.L.; Madishetty, K.; Guo, Y.; Woods, P.W.; Rooney-Latham, S.; Rascoe, J.; Gallindo, T.; Schnabel, D.; Polek, M. (2013) First Report of ‘Candidatus Liberibacter asiaticus’ associated with citrus huanglongbing in California. Plant Disease 97(2):283 [Abstract].

Li, W.; Hartung, J.S.; Levy, L. (2006). Quantitative real-time PCR for detection and identification of ‘Candidatus Liberibacter species associated with citrus huanglongbing. Journal of Microbiological Methods 66:104-115.

Slupsky, C.M.; Breksa, A.P.; Hilf, M. (2013) Metabolites may reveal attack strategy of the microbe causing HLB. Citrograph 4(1):40–42.

Darya Mishchuk, Ph.D., and Xuan He are research associates in Professor Slupsky’s lab, and Carolyn Slupsky, Ph.D., is a professor with a joint appointment in the Department of Nutrition and the Department of Food Science and Technology at the University of California, Davis. For more information, contact [email protected]

Field DataAddress, GPS coordinates, citrus

variety, collection date, ACP numbers, notes, etc.

Sample HandlingReceipt date, condition of

sample, sample preparation, data acquisition, data analysis

Searchable databaseKeep track of each sample from the moment it is collected until

�nal results

Unique sample identifier

Partial pattern matching

ResultsPredicted HLB infection

status

Step 1Simpli�ed sample processing. Extraction

adapted to automatic liquids handler.

Step 2Automated NMR data acquisition

(already available)

Step 3Metabolite identi�cation and

quantitation, and statistical analysis.

Figure 2. Method development for high-throughput metabolomics analysis. Step 1 (sample processing) is completed and ready to be tested with a liquids handler. Step 2 is already available. Step 3 needs to be completed for full high-throughput automation.


THERE’S NO ROOM FOR MITES OR ACP.

©2017 Nichino America, Inc. All rights reserved. FujiMite and Nichino America logo are registered trademarks of Nichino America, Inc. Always read and follow all label directions. Refer to global MRL database for current established tolerances www.globalmrl.com/db#query | 888-740-7700 | www.nichino.net

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ACP Control in Southern CaliforniaWhole Orchard Studies of the Efficacy of Grower-applied Spring InsecticidesNastaran Tofangsazi, Beth Grafton-Cardwell and Enrico Ferro

Project Summary The residual control¹ of Danitol® 2.4 EC, Actara® WG and Entrust® SC insecticides against Asian citrus psyllid (ACP) during late winter (February – air applications) and early spring (March – ground applications) 2016 were studied in Southern California. When applications were made by air in February, all tested insecticides suppressed adults and nymphs below two per sweep or flush on most dates for the first 45 days. As applications were made by ground in March, when leaves had expanded and the densities of nymphal pysllids were on average higher, Danitol and Actara suppressed nymphs and adults below two on most dates during 94 days of sampling, while Entrust provided 2-13 days of adult and nymph suppression. Similar to our previous study in fall 2015 (Tofangsazi et al. 2015), Actara was the most consistently effective insecticide for controlling ACP nymphs by air and ground application. This study provides new information regarding the persistence of current insecticides used for ACP control during early spring, which is helping to shape the ACP Integrated Pest Management (IPM) program for commercial citrus in southern California.



Introduction The ACP poses a significant threat to California’s citrus industry due to their ability to transmit the bacterium, ‘Candidatus Liberibacter asiacticus,’ associated with the deadly citrus disease, huanglongbing (HLB). Currently, growers rely heavily on chemical control of ACP in both conventional and organic groves. Understanding the level of ACP reduction and the duration of insecticide residual control under field conditions are critical components of ACP/HLB management.

Controlling ACP adults using foliar insecticide applications during tree dormancy throughout the winter (December-February), following fall flush and prior to the initiation of spring flush, is one of the most important and effective ACP management practices. During winter, citrus foliage hardens off and the eggs and nymphs do not survive well. Thus, the adult is the primary stage found at this time of year. As soon as spring flush appears, over-wintering adult psyllids reproduce freely on new flushes. If these populations are not brought under control before eggs and nymphs appear, they are more difficult to control later in the season. During the winter, ACP natural enemies are less active and less likely to be exposed to insecticides. Thus, outbreaks of secondary pests are less likely to happen when treatments are applied between December and February.

This study’s purpose was to determine the effectiveness of the pyrethroid Danitol 2.4 EC (fenpropathrin), the neonicotinoid Actara WG (thiamethoxam) and the organic insecticide Entrust SC (spinosad) for the control of psyllids in the early spring when applied by air and by ground.

Experimental ProtocolTo determine the level of insecticide residual control during early spring, ACP populations (eggs, nymphs and adults) were monitored from February 9 (pre-treatment) to early spring (post-treatment) 2016 at 7-14 day intervals after a grower in Pauma Valley, San Diego County, treated six orchards. Three flushes were randomly collected from five trees along two border rows and a center row in each orchard (15 flushes per row, 45 flushes per orchard), ensuring that flushes were not taken from adjacent trees. Newly-formed flushes were inspected under a dissecting microscope to determine ACP egg and nymph densities, and ACP adult densities were determined by sweep net sampling2 three times on three different sides of the same trees sampled for flushes. The mean numbers of adult psyllids per sweep and nymphs and eggs per flush were recorded.

Air and ground applications were applied four weeks apart. Three orchards received aerial treatments (Danitol, Actara, Entrust) applied by helicopter in 50 gallons per acre (gpa), and three orchards received ground applications using an Aerofan airblast sprayer applied in 400 gpa water. The label rate of each insecticide treatment was applied to each orchard without untreated areas as follows:

Figure 1. Impact of air application of Danitol 2.4 EC on the average number of adult ACP captured per sweep net per tap, and the nymphs and eggs per flush in whole orchard studies with grower-applied treatments.

Figure 2. Impact of air application of Actara WG on the average number of adult ACP captured per sweep net per tap, and the nymphs and eggs per flush in whole orchard studies with grower-applied treatments.

Figure 3. Impact of air application of Entrust SC with 1% BFR 440 Supreme Spray Oil on the average number of adult ACP captured per sweep net, and the nymphs and eggs per flush in whole orchard studies with grower-applied treatments.


Treatments applied on February 16, 2016, by air in 50 gpa

Danitol 2.4 EC, 21 oz/acre (fenpropathrin, Valent USA Corp.)

Actara WG, 5.5 oz/acre (thiamethoxam, Syngenta Crop Protection)

Entrust SC, 9 oz/acre (spinosad, Dow AgroSciences + 1% BFR 440 Supreme Spray Oil)

Treatments applied on March 22, 2016, by ground (400 gpa)

Danitol 2.4 EC, 21 oz/acre

Actara WG, 5.5 oz/acre

Entrust SC, 9 oz/acre + 1% BFR 440 Supreme Spray Oil

Results and DiscussionFigures 1–3 show the mean number of adult ACP sampled by sweep net and the average number of nymph and eggs per flush per orchard for the Danitol, Actara and Entrust air applications. The Danitol treatment suppressed all stages below one per sweep or flush for 31 days, at which time the eggs and nymphs began to increase indicating that the residual impact of the pesticide had declined (Figure 1). Relatively high egg densities (six per flush) were found when flush was sampled prior to treatment with Actara, indicating that the February 16 treatment was applied after egg laying had begun (Figure 2). Actara and Entrust treatments suppressed nymphs and egg stages below two per sweep or flush through 50 days of sampling (Figures 2 and 3).

Figures 4–6 show the mean number of adult ACP sampled by sweep net and the mean number of nymphs and eggs per flush for ground treatments, which were applied on March 22 after flush had expanded and psyllid populations were established. Ground application of Danitol suppressed nymphal populations to nearly undetectable levels for 49 days after treatment (Figure 4). Eggs were found at low levels (one to three eggs per sampling period) during the same 49 days after treatment. The Actara ground application had a strong impact on all stages, reducing the population to levels of no more than two psyllids at each development stage per sweep or flush through 94 days post treatment – excluding day 13 (Figure 5). In contrast, the Entrust ground treatment only surpressed egg and nymph counts through day 13; at the next sample point, their numbers began to increase (Figure 6).

Of the three stages sampled, nymphal counts provided the most reliable information regarding residual efficacy of insecticides for ACP control. In mid-February, nymphal populations were zero to two per flush in the three sites (Figures 1-3). All three insecticides applied by air in mid-February reduced or kept psyllids below two per leaf on most dates for 45-50 days. In March, immature psyllid densities

Figure 5. Impact of ground application of Actara WG on the average number of adult ACP captured per sweep net, and the nymphs and eggs per flush in whole orchard studies with grower-applied treatments.

Figure 4. Impact of ground application of Danitol 2.4 EC on the average number of adult ACP captured per sweep net, and the nymphs and eggs per flush in whole orchard studies with grower-applied treatments.

Figure 6. Impact of ground application of Entrust SC with 1% BFR 440 Supreme Spray Oil on the average number of adult ACP captured per sweep net, and the nymphs and eggs per flush in whole orchard studies with grower-applied treatments.

1.2.

3.

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tended to be higher (1-14 nymphs/flush), and a ground application of Entrust was less successful in suppressing the population below two nymphs per flush compared to Danitol or Actara. In fall 2015 (Tofangsazi et al. 2016), the nymph population was much higher (15-30 nymphs per flush in eight of ten sites) compared to the spring 2016 populations in the study. Entrust was less effective in reducing ACP in the fall compared to Actara.

These results suggest that the efficacy of Entrust decreases with increasing psyllid density, likely because it has very short residual activity and must make direct contact with the psyllids. This also suggests that repeat applications of Entrust are needed to reduce psyllid numbers to a level comparable to a conventional insecticide when psyllid populations are high (after winter). Since the maximum number of applications of Entrust is only three times per calendar year, one application of Entrust during winter/early spring and two applications during the growing season applied within 10-14 days of each other or alternated with another insecticide would be the best use of this product.

Based on these results, both aerial and ground applications of the tested insecticides may be good options for ACP control in early spring. Treatments should be applied as early as possible, preferably in January. After February, higher ACP numbers make control more difficult, especially with for those products with short residual activity.

Future PlansFuture studies will be designed to more directly compare air and ground applications of these insecticides for effective ACP control. We also are very interested in studying the role of orchard borders on ACP population densities. CRB Research Project #5500-189

This project is supported in part by Citrus Research Board funding and USDA TASC funding. Field and laboratory assistance were provided by Brandon Skylar Rogers, Imon Riaby and Clarisa León.

Glossary¹Residual control: The amount of time after field application that an insecticide is effective in killing pests.

2Sweep net sampling: Placing a citrus tree branch into a sweep net and shaking it vigorously to dislodge psyllids into the net.

ReferencesGrafton-Cardwell, E.E.; Morse, J.G.; O’Connell, N.V.; Phillips, P.A.; Kallsen, C.E.; Haviland, D.R. 2015. UC IPM Pest Management Guidelines: Citrus. UC ANR Publication 3441.

Tofangsazi, N.; Grafton-Cardwell, E.; Rogers, B.; Ferro, E. 2016. Efficacy of grower applied fall insecticide treatments for Asian citrus psyllid in Southern California. Citrograph 7(4):50-54.

Nastaran Tofangsazi, Ph.D., is a post-doctoral scholar in the Department of Entomology, University of California, Riverside. Beth Grafton-Cardwell, Ph.D., is an integrated pest management specialist with the University of California, Riverside and the Director of the Lindcove Research and Extension Center. Enrico Ferro is the San Diego County grower liaison for the California Department of Food and Agriculture ACP task force. For additional information, contact [email protected]

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Phytophthora syringae and New Fungicides for Managing Brown RotJames Adaskaveg, Helga Förster, Wei Hao and Morgan Gray

Project SummaryCurrently, Phytophthora syringae and P. citrophthora are the predominant species causing brown rot during the winter season in California. In many orchards, only P. syringae was detected. The ecology of P. syringae is being studied to determine survival mechanisms and inoculum sources of the pathogen. Soil sampling only recovered P. citrophthora even when P. syringae was the major cause of fruit brown rot. Furthermore, P. syringae was rarely recovered from citrus roots. This led to a search of other ecological niches and the discovery that P. syringae is present in leaf litter under trees during the cooler months of the year. Research is ongoing to elucidate the time when leaf litter is colonized. New pre-harvest foliar treatments of mandipropamid (Revus®) and oxathiapiprolin (Orondis®) were evaluated and compared to copper and phosphite. Harvested fruit were inoculated with P. citrophthora or P. syringae at selected intervals after treatment. Revus and Orondis generally out-performed phosphite and copper, lasted over an eight-week period under natural rainfall conditions at multiple trial sites and will be federally registered for foliar application in 2018.


Brown rot on tree.


Citrus brown rot is caused by several species of Phytophthora, a genus of fungal-like organisms. Although Phytophthora species cause plant diseases similar to true fungi, they belong to their own kingdom of organisms (Stramenopila; phylum Oomycota). In California, P. parasitica and P. citrophthora were considered the most important species causing brown rot in the past (Feld et al. 1979), and P. citrophthora was regarded as the winter pathogen (Menge et al. 1988). Based on our surveys starting in 2013 and continuing through 2017, however, P. syringae is now the predominant species in many orange orchards in the Central Valley (District 1), and P. citrophthora is the second most common species. Our surveys are now extending into District 2 (coastal region). Phytophthora syringae and P. hibernalis are currently quarantined plant pathogens in some international export markets (e.g., China), warranting more extensive research efforts on pathogen biology and disease management.

Symptoms of citrus brown rot, regardless of causal species, are brown discoloration of the rind, a leathery decay texture and a distinctive, pungent odor. At high relative humidity, white fungal growth covers the fruit surface. Losses from brown rot can result from pre-harvest infections in the orchard and from post-harvest fruit decay. Fruit in transit may develop symptoms from non-visible infections. In tight-filled boxes, fine fungal threads (mycelium) may grow from infected fruit to adjacent fruit, increasing losses.

Biology of Phytophthora species Phytophthora species are primarily known as soil-borne organisms1 causing root rots and trunk cankers (Graham and Menge 2000). Fungal propagules2 can be splashed from the soil into the tree and infect fruit, thus causing brown rot. Some species (P. syringae and P. citrophthora) mostly infect low-hanging fruit because their sporangia (fungal spore-bearing stems) do not easily detach from the mycelium; whereas other species (P. hibernalis and some species that do not occur in California) infect fruit all over the tree because their sporangia easily separate from the mycelium and can be wind-disseminated. Phytophthora hibernalis occurs in California, and brown rot may develop on fruit all over the tree. Thus, management guidelines include whole-tree applications of fungicides if fruit are to be shipped to markets with quarantine restrictions.

SurveysA total of 1,638 oranges with brown rot symptoms were collected from orchards in Fresno and Tulare counties between winter 2013 and summer 2015. In the winter surveys in both counties, orange brown rot was determined to be primarily caused by P. syringae (Figure 1) and incidence among isolates ranged from 73.6 percent (Fresno County 2014) to 96.1 percent (Tulare County 2013). The remaining isolates were identified as P. citrophthora. In contrast, in late spring/summer samplings, only P. citrophthora was detected in diseased fruit (Figure 1). Phytophthora parasitica and P. hibernalis were not detected.

Phytophthora species were identified after isolation from diseased fruit using macro- and microscopic cultural characteristics, as well as molecular techniques – Random Amplified Polymorphic DNA patterns and TaqMan® qPCR. The qPCR method3 was found to be the quickest method and also was more sensitive, successfully detecting Phytophthora spp. in some samples where isolation was not successful.

Source of Pathogen PopulationsWe also collected roots and rhizosphere soil (the soil immediately adjacent to the roots) in ten orchards to determine the population levels of the two major brown rot pathogens. Direct isolation, soil dilution plating and baiting techniques4 were used. For the baiting technique, soil samples were placed in plastic bags, water was added and a green pear was added (Figure 2A). In successful baitings, firm, brown lesions developed on the skin of each fruit (Figure 2B), which were determined to be caused by Phytophthora spp. Phytophthora citrophthora was recovered from the rhizosphere in all locations, even when only P. syringae was detected in fruit with brown rot. Surprisingly, P. syringae was present at only low incidence in rhizosphere soil and never in roots.

Orange leaf litter from the same orchards was baited using pears, and P. syringae was detected at high levels in nine locations.

Winter 29 orchards, 63 isolates

Late spring/summer 28 orchards, 63 isolates

Fig. 1. Average incidence of Phytophthoraspecies recovered from orange fruit with brown rot in the Central Valley of California in the winter and late spring/summer seasons in 2014 and 2015 .

P. syringae – 78%

Bothspecies– 4%

P. citrophthora – 18%

P. syringae – 0%

P. citrophthora – 100%

Figure 1. Average incidence of Phytophthora species recovered from orange fruit with brown rot in the Central Valley of California in the winter and late spring/summer seasons in 2014 and 2015 .


Phytophthora citrophthora was found in only one location. Phytophthora spp. was not recovered from living leaves.

Phytophthora parasitica and P. citrophthora are known citrus root pathogens and are readily recovered in platings of citrus soil (Erwin and Ribeiro 1996; Hao et al. 2016a). Phytophthora syringae, however, has never been isolated from citrus roots (Hao et al. 2016a). The low recovery rate from rhizosphere samples may be due to leaf litter contamination. The epidemiology of P. syringae is largely unknown because this species previously was considered a minor problem in citrus. Our epidemiological studies demonstrate that P. syringae mostly resides in leaf litter, occasionally in soil, but never in roots of citrus trees. Phytophthora syringae also causes pruning wound cankers on almond and was previously recovered from almond leaf litter (Doster and Bostock 1988). We still have to determine when P. syringae infects citrus leaves, but our research is leading to a better understanding of its disease cycle and survival strategies. This information may result in new cultural practices such as leaf litter removal or chemical treatment to induce rapid degradation of organic material under a tree.

Current Disease Management ProgramsStrategies for brown rot control include irrigation management, skirting trees, not picking fruit from the lower tree canopy and

chemical treatments. Copper applied as copper sulfate or as fixed neutral formulations in a mixture with zinc sulfate and lime has proven to reduce the incidence of brown rot and other diseases such as Septoria spot. These applications are preventively done before the winter rains. One or two applications at the beginning and in the middle of the harvest season are highly effective under low rainfall conditions. In winters with high rainfall, two to three applications are required, with the third spray applied in March. Overuse of copper may result in its accumulation in soils, run-off surface waters, possible tree injury, and may lead to resistant populations of citrus pathogens. Therefore, non-copper-based alternatives are needed that can be used alone or in rotation with copper in highly effective and ecologically sustainable management programs.

Because Phytophthora species are not closely related to true fungi, modes of action5 have been developed specifically for these organisms. As alternative pre-harvest fungicides, currently only mefenoxam (Ridomil Gold®) and phosphonates such as potassium phosphite are available in California. Ridomil Gold is used as a soil treatment to reduce soil populations of the pathogens, whereas the systemic phosphonates can be applied to soil or directly to the tree. Unfortunately, resistance to Ridomil Gold has developed in many locations since its introduction in the 1980s. This led to overuse of phosphonates and to the recent detection of phosphonate resistance in P. parasitica, P. citrophthora and P. syringae in California citrus orchards. If phosphonates continue to be used without rotation with other modes of action, resistance will eventually increase, and these compounds will no longer be useful in disease management.

New Materials and Future DirectionsIn collaboration with the agrochemical industry, we are evaluating new fungicides for Phytophthora disease management. Four new fungicides (fluopicolide–Presidio®, mandipropamid–Revus, oxathiapiprolin–Orondis, ethaboxam–Intego Solo®), each representing a unique mode of action (FRAC Groups6 - FG 43, 40, U15, and U5, respectively), are being evaluated as foliar and/or soil treatments for managing brown rot and root rot (Adaskaveg et al. 2015; Hao et al. 2016b). The four fungicides are highly toxic to Phytophthora spp. and have been performing well in multiple trials in reducing soil populations and root rot caused by P. parasitica and P. citrophthora. We are pursuing Revus and Orondis as foliar and soil treatments so that new modes of action can be integrated with copper and phosphonate pre-harvest foliar treatments.

Brown Rot Management Field Trials The persistence of fungicides on citrus was evaluated in Navel orange groves at the University of California, Riverside and the Kearney Agricultural Research and Extension Center during the winter. A single treatment was applied in the first week of January. Fruit were sampled after every rain event over an eight-week period and inoculated with P. citrophthora or P. syringae. Presidio, Revus and Orondis were evaluated and compared to copper (FG M1) (Badge SC112 fl oz + Lime 3.5 lb) and ProPhyt® (FG 33). Revus

Fig.2.D’Anjou pearsusedasbaittorecoverPhytophthora spp.fromleaflitterandsoilsamples.A.Fruitinplasticbagsincubating.B.Fruitafter14daysofincubationat12°C(54°F).Thefruitontheleftshowsanearlystageofinfection,whereastheothertwofruitshowadvancedsymptoms.

A

B

Figure 2. D’Anjou pears used as bait to recover Phytophthora spp. from leaf litter and soil samples. A. Fruit in plastic bags incubating. B. Fruit after 14 days of incubation at 12°C (54°F). The fruit on the left shows an early stage of infection, whereas the other two fruit show advanced symptoms.


and Orondis (both Syngenta Crop Protection) were highly effective over a five-week period and significantly reduced the incidence of brown rot of fruit inoculated by both pathogens, similar to or better than copper (Badge SC 112) (Figure 3). After eight weeks, brown rot caused by P. citrophthora was still reduced by 48 percent (Revus) or 75 percent (Orondis) as compared to the control. After inoculation with P. syringae, brown rot was reduced by more than 75 percent using all fungicides evaluated. In contrast, the activity of ProPhyt for managing P. citrophthora declined rapidly and was greatly reduced after the first rain events (Figure 3).

Based on our efforts, Revus is in the IR-4 federal specialty crop registration program (http://www.apsnet.org/publications/apsnetfeatures/Pages/TheIR4Project.aspx) for pre-harvest treatments of citrus. Orondis is being registered directly by Syngenta for soil and foliar applications on citrus. California registrations are pending expected federal registration, which is 2018 for both fungicides. Additionally, based on the successful use in our Phytophthora root rot trials, Intego and Presidio will be registered as soil applications on citrus (federal registration of fluopicolide is expected in 2017).


ReferencesAdaskaveg, J.E.; Förster, H.; Hao, W.; Cary, D. 2015. Managing citrus brown rot for export to China - From a chore to a necessity. Citrograph 6:36-40.

Doster, M.A.; Bostock, R.M. 1987. Quantification of lignin formation in almond bark in response to wounding and infection by Phytophthora species. Phytopathology 78:473-477.

Erwin, D.C.; Ribeiro, O.K. 1996. Phytophthora Diseases Worldwide. APS Press, The American Phytopathological Society, St. Paul, Minnesota.

Feld, S.J.; Menge, J.A.; Pehrson, J.E. 1979. Brown rot of citrus: a review of the disease. Citrograph 64:101–106.

Graham, J.H.; Menge, J.A. 2000. Phytophthora-induced diseases. p. 12–15. In: L.W. Timmer, S.M. Garnsey, and J.H. Graham, (eds.), Compendium of Citrus Diseases. APS Press, The American Phytopathological Society, St. Paul, Minnesota.

Hao, W.; Förster, H.; Miles, T.; Martin, F.; Browne, G.; Adaskaveg, J. 2016a. A leaf litter and fruit brown rot life style of Phytophthora syringae in California citrus. Phytopathology 106:S4.132.

Hao, W.; Gray, M.; Förster, H.; Adaskaveg, J.E. 2016b. Evaluation of new fungicides for management of Phytophthora root rot of citrus. Phytopathology 106:S4.2.

Menge, J.A. et al. 1988. Distribution and frequency of Phytophthora parasitica and P. citrophthora associated with root rot of citrus in California. Phytopathology 78:1576.

Glossary¹Soil-borne organisms: Organisms that live in the soil for most of their life.

2Propagule: Structure like a spore that disseminates or propagates the organism.

3qPCR: Molecular method based on PCR that quantifies target DNA.

4Baiting technique: Method to recover a microorganism from an environmental sample using a food source.

5Mode of action: Specific change in a living organism at the cellular level that results from the exposure to a chemical.

6FRAC groups: Code on a fungicide label and a number assigned by the Fungicide Resistance Action Committee (FRAC) to group together active ingredients that demonstrate potential for cross resistance.

James Adaskaveg, Ph.D., is a professor of plant pathology at the University of California, Riverside. Helga Förster, Ph.D., is a project scientist in plant pathology at the University of California, Riverside. Wei Hao, Ph.D., is a post-doctoral researcher at the University of California, Riverside. Morgan Gray is a doctoral candidate in plant pathology at the University of California, Riverside. For more information, contact [email protected]

Figure 3. Temporal efficacy of pre-harvest treatments for management of Phytophthora brown rot of navel oranges at UC Riverside winter 2015. Treatments were applied on January 23, 2015, at a rate of 400 gal/A. Fruit were harvested periodically over two months and inoculated with P. citrophthora or P. syringae.

Fig.3.Temporalefficacyofpre-harvesttreatmentsformanagementofPhytophthorabrownrotofnavelorangesatUCRiversidewinter2015.TreatmentswereappliedonJanuary23,2015,atarateof400gal/A.FruitwereharvestedperiodicallyovertwomonthsandinoculatedwithP.citrophthoraorP.syringae.

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Compatibility of Organic and Conventional Insecticides to Tamarixia radiataJawwad Qureshi and Philip Stansly


Project SummaryManagement of the Asian citrus psyllid (ACP) vector of the huanglongbing (HLB)-associated bacterium, using biological and chemical control is critical for developing integrated and sustainable area-wide control of this vector. Tamarixia radiata, an ecto-parasitoid of ACP nymphs, is mass produced and released in Florida, California and Texas. We are evaluating Tamarixia release in commercial citrus groves using organic and conventional insecticides to enhance ACP control.

In 2015 and 2016, 13 and eight spray applications were made in organic programs, respectively, and eight and six applications in the conventional program, respectively. A total of 94,764 (2015) and 118,386 (2016)

Figure 1. Asian citrus psyllid adult (Photo by J. Qureshi).


Tamarixia adults were released. Another experiment conducted in 2015 received nutritional sprays and only three applications of conventional insecticides and a total release of 44,050 Tamarixia.

Tamarixia were recovered throughout the growing season in all programs, although more consistently in organic or untreated blocks compared with conventional blocks. Parasitism averaged 15-31 percent in the untreated control, 11-24 percent in the organic programs and 0-3 percent in the conventional program in 2015 and 13-22 percent in the untreated control, 8-32 percent in the organic programs and 0-6 percent in the conventional program in 2016. When less conventional insecticides were used, parasitism averaged 0-13 percent. Consistent mass releases of Tamarixia may provide useful additional control where conventional and especially organic insecticides are used to control ACP.

BackgroundHLB, associated with the bacterium ‘Candidatus Liberibacter asiaticus’ (CLas) and vectored by ACP, is considered the most damaging of all citrus diseases. The ACP adult (Figure 1) is responsible for spreading CLas through its movement, whereas nymphs (Figure 2) primarily acquire the bacterium. Insecticidal and biological control are two important components of citrus pest management. Sole reliance on a single method of control is not enough.

Biological control is generally the first line of defense against invasive pests, including ACP. Tamarixia radiata are tiny parasitic wasps that co-evolved over time with ACP in tropical and subtropical Asia. Tamarixia females lay eggs under ACP nymphs (generally one egg per nymph) in the third to early fifth instar phase from which the Tamarixia adults emerge instead of ACP (Figure 2). Female wasps also may feed on young nymphs. Each female is capable of destroying up to 500 nymphs during her lifetime.

Tamarixia were released in Réunion, Taiwan and Guadaloupe, and was credited with reducing ACP populations sufficiently in Réunion to mitigate HLB impact. The parasitoid also were detected in Brazil and Puerto Rico, where no known releases were made. At Isabela, Puerto Rico, parasitism generally exceeded 50 percent and averaged 70 percent for the year. More importantly, parasitism ranged from 79-88 percent between January and April followed by a significant and persistent decline in psyllid populations, indicating that Tamarixia have the potential to reduce ACP under conditions suitable for their survival.

Tamarixia, imported from Taiwan, Pakistan, mainland China and Vietnam, are now mass produced and released in Florida while Tamarixia from Pakistan are now produced and released in California and Texas to help suppress ACP. Knowledge of compatibility with insecticides is useful in improving Tamarixia performance in environments where insecticides are used, such as commercial citrus, and in developing integrated and sustainable pest control methods to reduce ACP and HLB. We evaluated Tamarixia releases for their establishment and impact in commercial citrus that employed organic and

Figure 2: Asian citrus psyllid nymphs and female Tamarixia radiata in the center laying an egg on an ACP nymph (Photo by J. Lotz).


conventional chemical control of ACP and nutritionals to improve tree health.

Psyllid Control Programs, Tamarixia Release and EvaluationThree organic programs, (1) organic insecticides only, or organic insecticides tank mixed and rotated with either (2) horticultural mineral oil (FL 435-66) or (3) with insecticidal soap (M-pede), and a conventional program are being evaluated in a 15-acre block of Valencia oranges in Hendry County, Florida, for control of ACP. Thirteen spray applications in each organic program and eight in the conventional program were made during 2015. In 2016, eight and six sprays were made in organic and conventional programs, respectively.

A total of 94,764 Tamarixia adults averaging 7,897 per month in 2015 and 118,386 averaging 9,866 per month in 2016 were equally distributed across all programs including the untreated controls. Shoots containing third to fifth instar nymphs of ACP were randomly collected from trees in each replicate, labeled and transported in an insulated cooler to the laboratory where they were kept in ventilated containers (Figure 3) and held at ambient temperature for at least two weeks to allow adults of ACP and Tamarixia to emerge. Parasitism rates (percentages) were calculated based on the ratio of the number of emerged adult Tamarixia to the total combined number of adult ACP and Tamarixia that emerged from samples of nymphs reared from field collected shoots.

In 2015, Tamarixia releases also were evaluated in Collier County, Florida, in a 12-acre block of Hamlin oranges to

determine the impact of (1) nutritional sprays, (2) conventional insecticide sprays and (3) a combined nutritional and insecticidal spray on ACP and HLB.

Only three insecticide sprays were made. A total of 44,050 Tamarixia adults, averaging 4,405 per month, were released.

2015 Research FindingsNymphs were available to evaluate parasitism by Tamarixia in March, June, July and August. Parasitism averaged 31 percent in the untreated controls in March and 24 percent across all organic programs (Figure 4). Fewer nymphs were found in the conventional program, and none were parasitized. Parasitism rates dropped in June, averaging 17 percent in the untreated control trees, 11 percent across all organic programs and only three percent in the conventional program (Figure 4). Populations of nymphs increased on trees treated with the conventional program compared with samples collected in March from the same program, but most were not parasitized. The same was true in July, and none were parasitized, whereas parasitism in untreated and organic programs averaged 15 percent and 18 percent, respectively (Figure 4). Nymphs were rare in August except for the untreated control trees and organic program 1, averaging 19 and 24 percent parasitism, respectively (Figure 4). In September, nymphs were not available from untreated control trees or from trees in any of the treatments.

In the Collier County block of Hamlin oranges, nymphs were present in March, July, September and October. Parasitism was observed in all programs from March to October averaging 0-20 percent in program 1, 0-13 percent in program

Figure 3: Rearing of ACP nymphs under ventilated cylinders for emergence of ACP adults and Tamarixia radiata to calculate percentage parasitism (Photo by J. Qureshi).


2, and 0-9 percent in program 3, respectively, compared with 15-29 percent in the untreated (Figure 5).

2016 Research Findings Nymphs were found for evaluation in all programs in March 2016. Parasitism averaged 17 percent in the untreated, and nine percent in organic programs (Figure 6). No parasitoids emerged from nymphs reared from trees in organic program 3 or the conventional program. In April, parasitism averaged 13 percent in the untreated, eight percent in organic programs and six percent in the conventional program (Figure 6). In June, parasitism averaged 22 percent in the untreated controls, and 32 percent across organic programs (Figure 6). Nymphs for evaluation were not available from organic program 3 and the conventional program.

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7 2 5.17 08.92 5.33 0 8.692.43 0 9.43 04.16 10.3 0 8.43

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tparasitism

2015

UntreatedNutritiononlyspraysInsecticideonlyspraysInsecticideplusnutritionsprays

Figure 4. Mean (±SE) percent parasitism by Tamarixia radiata in organic and conventional programs employed to control Asian citrus psyllid. In August, SE is not presented for organic programs because nymphs were available only in one of the three organic programs used to calculate SE.

Figure 5. Mean (±SE) percent parasitism by Tamarixia radiata in nutritional and insecticide spray programs employed to control Asian citrus psyllid and improve tree health. In October, SE is not presented for insecticides only spray program because nymphs were available only from one of the four replicates used to calculate SE.

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Establishment and Impact of Tamarixia These results suggest that with consistent mass releases, Tamarixia have the potential to establish and negatively impact ACP in organic and, to a lesser extent, in conventional programs. This is useful for California and other locations where commercial citrus producers rely on chemical control. An increasing trend of parasitism was observed even with the conventional programs when the number of spray applications was reduced. More sprays are not always recommended for sustainable crop protection and production, particularly in systems such as California’s and Florida’s where multiple pests are present and kept under check by several biological control

agents. Citrus production systems that rely on intensive calendar-based spray applications of insecticides continue to see disease spread, diminishing biological control, increased pesticide resistance and risk of contaminated environment. Therefore, mass production and release of Tamarixia are an option to augment natural populations and reinforce insecticidal control of ACP in both organic and conventional programs.


AcknowledgementsWe would like to thank the Citrus Research Board for funding this research and the Florida Department of Agriculture and Consumer Services, Division of Plant Industry for providing Tamarixia radiata.

Jawwad Qureshi, Ph.D., is an assistant professor of entomology, and Phil Stansly, Ph.D., is a professor of entomology, both with the University of Florida-Institute of Food and Agricultural Sciences at the Indian River Research and Education Center at Fort Pierce and Southwest Florida Research and Education Center at Immokalee, respectively. For additional information on this subject, please contact [email protected]

0

10

20

30

40

Mar Apr Jun

Percen

tparasitism

2016

UntreatedOrganicprogramsConventionalprogram

Figure 6. Mean (±SE) percent parasitism by Tamarixia radiata in organic and conventional programs employed to control Asian citrus psyllid.

Table 1: Schedule of insecticidal sprays and Tamarixia radiata releases in the experiment evaluating organic and conventional programs for ACP control.

Organic Program 1 Organic Program 2 Organic Program 3 Conventional Program Number of Year Month Organic insecticides Organic insecticides + Organic insecticides + Synthetic insecticides Tamarixia releases

applicationa 1, 2, 3 M-pede (M) 2% v/v 435 oil (O) 2% v/v applicationa 1, 2, 3 in the monthb

applicationa 1, 2, 3 applicationa 1, 2, 3

2015 January 1 Pyganic 1 Pyganic (M) 1 Pyganic (O) 1 Danitol 2February None None None None 2March 1 Aza-Direct 1 Aza-Direct (M) 1 Aza-Direct (O) 1 Closer 4April 1 Grandevo, 2 Azera 1 M-pede, 2 Azera (M) 1 435 oil, 2 Azera (O) 1 Movento, 2 Micromite 1May 1 Venerate, 2 Entrust 1 M-pede, 2 Entrust (M) 1 435 oil, 2 Entrust (O) 1 Imidan 2June None None None None 1July 1 Surround, 2 M-pede, 3 Microthiol 1 M-pede, 2 M-pede, 3 Microthiol 1 435 oil, 2 M-pede, 3 Microthiol 1 Dimethoate 2August 1 Azera 1 M-pede 1 435 oil 1 Baythroid 2September 1 Grandevo 1 Grandevo (M) 1 Grandevo (O) Apta 2October None None None None 1November 1 Pyganic 1 Pyganic (M) 1 Pyganic (O) None 2December 1 Pyganic 1 Pyganic (M) 1 Pyganic (O) None 2

2016 January 1 Pyganic 1 Pyganic (M) 1 Pyganic (O) 1 Danitol 3February None None None None 5March 1 Aza-Direct 1 Aza-Direct (M) 1 Aza-Direct (O) 1 Sivanto 3April 1 Surround 1 M-pede 1 435 oil 1 Exirel 4May 1 Azera 1 Azera (M) 1 Azera (O) 1 Actara 3June 1 Grandevo 1 M-pede 1 435 oil 1 Mustang Max 4July 1 Venerate 1 Venerate (M) 1 Venerate (O) 1 Imidan 4August None None None None 5September None None None None 2October None None None None 3November 1 Pyganic 1 Pyganic (M) 1 Pyganic (O) None 5December 1 Pyganic 1 Pyganic (M) 1 Pyganic (O) None 3a Number indicate first 1 (first), 2 (second) and 3 (third) spray application made during the month followed by the productb Number indicate times Tamarixia radiata were released, per month average of 7,897 adults in 2015 and 9,866 adults in 2016 were released

Table 1: Schedule of insecticidal sprays and Tamarixia radiata releases in the experiment evaluating organic and conventional programs for ACP control.

a Numbers indicate first 1 (first), 2 (second) and 3 (third) spray application made during the month followed by the productb Numbers indicate times Tamarixia radiata were released, per month average of 7,897 adults in 2015 and 9,866 adults in 2016 were released


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