OCTOBER–DECEMBER 2014 • VOLUME 68 NUMBER 4 California Agriculture

Endemic and Invasive Pests and Diseases: How UC and its collaborators detect, contain and manage them

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98 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 TABLE OF CONTENTS OCTOBER–DECEMBER 2014 • VOLUME 68, NUMBER 4 Endemic and Invasive Pests and Diseases: How UC and its collaborators detect, contain and manage them News departments 100 Editorial UC and the state of California team up against invasive species Grafton-Cardwell et al. COVER: Across the United States, endemic and invasive pests are a growing problem 102 Research news that costs billions of dollars each year Unwelcome arrivals in direct damage and funding for pest Warnert management programs. In California, UC ANR researchers collaborate with 105 Ongoing research state and federal agencies to contain and manage pests such as glassy-winged A look at EIPD Strategic Initiative projects sharpshooter, European grapevine moth White and herbicide-resistant weeds. In this 102 105 photo, Elizabeth Karn, Ph.D. student (left), and Associate Professor Marie Collaborations Jasieniuk (right) of UC Davis cross glufosinate-resistant Lolium (ryegrass) Excluding Pests and Pathogens plants with glufosinate-susceptible plants to determine whether the resistance 109 Diagnostics in animal health: How UC helps exclude and trait can be transmitted to offspring. The minimize impact of livestock pathogens results of their research will help inform Adaska et al. resistance management strategies. Photo by Will Suckow. 117 Plant health: How diagnostic networks and interagency partnerships protect plant systems from pests and pathogens Bostock et al. 109 117 About this issue Managing Newly Established Pests This special issue of California 125 Growers, scientists and regulators collaborate on European Agriculture highlights the UC Division grapevine moth program of Agriculture and Natural Resources’ Cooper et al. work on endemic and invasive 134 Collaborative efforts contained spread of Pierce’s disease pests and diseases that threaten and found genetic resistance the state’s people, agriculture and Bruening et al. 125 134 natural resources. The commitment to research and outreach profiled Maintaining Long-term Management inside includes the EIPD Strategic 142 Herbicide-resistant weeds challenge some signature Initiative, the UC Statewide IPM cropping systems Program and historic and ongoing Hanson et al. successful collaborations with 153 Over 35 years, integrated pest management has reduced regulatory agencies and the pest risks and pesticide use agricultural community. California Goodell et al. 142 153 Agriculture gratefully acknowledges the EIPD leaders for this special issue: Elizabeth Grafton-Cardwell E-edition research article (Cooperative Extension Specialist This article can be found in full on the California Agriculture and Research Entomologist, website; for a summary and link, see page 158. Department of Entomology, UC 158 The cost of the glassy-winged sharpshooter to Riverside) and Cheryl Wilen (IPM California grape, citrus and nursery producers Advisor, UC Statewide IPM Program Jetter et al. and UCCE San Diego County). The spread of GWSS in the late 1990s led to increased costs and changes in agricultural practices for grape, citrus and nursery producers. 158

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 99 Editorial UC and the state of California team up against invasive species

n recent years, the escalation of world travel has extension programs continue, supported by grant rapidly moved pests and pathogens to new regions funds from UC ANR, CDFA, commodity groups and Iand allowed them to invade and establish. This other sources. places enormous pressure on existing pest manage- Exclusion. Exclusion includes diagnostics, detec- ment systems and provides many challenges for tion and interception. With an early detection system research, regulatory agencies and outreach. It is esti- in place, the eradication of invading pests and dis- mated that the direct damage costs combined with the eases may be feasible. Lack of early detection often costs of controlling invasive species exceeds $138 bil- results in establishment, high management costs and Elizabeth E. Grafton- lion per year in the United States. Invasive species also disruption of trade and commerce. In the case of dis- Cardwell impact natural ecosystems, affecting, in the long term, eases, a lack of early detection may impact human or Cooperative Extension the diversity of our biological systems. animal health. UC and CDFA commit major resources Specialist and Research In 2009, as part of UC Agriculture and Natural to early detection. It’s UC ANR’s role to provide Entomologist Resources’ (UC ANR) 2025 Strategic Vision, five stra- science-based information to support exclusion strate- University of California tegic initiatives were established to focus UC ANR’s gies and inform policy and to assist with the detec- research and extension programs and increase its tion of new pests. This may take the form of assisting ability to address challenges that face California. The regulatory agencies with risk assessments, developing goal of the Endemic and Invasive Pests and Diseases innovative technologies for rapid identification and (EIPD) Strategic Initiative is to coordinate and support trapping, developing models of invasion biology for research and extension efforts on new and emerging predictive purposes and studying how the changing biological threats to California’s healthy food sys- climate or a local environment influences the intro- tems, natural resources and communities. The EIPD duction of pests and pathogens. Initiative focuses on (1) the exclusion of pests and CDFA’s Plant Pest Diagnostics Branch (PPDB) Annette Jones pathogens, (2) rapid response to emerging problems scientists provide identification of plant pests and with pests and diseases and (3) integrated manage- pathogens in their Sacramento laboratory. The PPDB State Veterinarian and Director, Animal ment of established pests. is the largest state plant diagnostic laboratory in the Health and Food Safety This issue of California Agriculture highlights United States. Samples may be collected by first detec- Services some of those UC research and extension efforts. UC tors trained through the Western Plant Diagnostic California Department programs studying crops and animal health have Network (WPDN) housed at UC Davis (page 117) and of Food and Agriculture provided critical scientific information and outreach submitted to a UC Cooperative Extension office or the to bring pests (insects, nematodes, weeds and verte- county agricultural commissioner. Samples not iden- brates) and pathogens (viruses, fungi, protozoans and tified at the county level are sent to the Sacramento bacteria) under significant control. However, UC does laboratory. UC ANR scientists, such as Valerie not conduct these efforts alone. The work to combat Williamson at UC Davis, play a role in developing invasive and endemic species relies heavily on team- diagnostics tools; Williamson is using mitrochondrial work between UC and state and/or federal regulatory DNA to identify invasive and endemic root knot nem- agencies; these collaborations have proved critical for atodes that attack crops. managing pests and pathogens and protecting the UC and CDFA have also worked together closely state’s agriculture industry, homeowners’ gardens, to ensure growers have access to clean planting stock. Nick Condos California’s wildlands and human health. UC ANR is home to the Citrus Clonal Protection Director, Plant Health In particular, UC and the California Department of Program, directed by Georgios Vidalakis, and the and Pest Prevention Division Food and Agriculture (CDFA) have together created Foundation Plant Services program, directed by California Department a powerful team to limit the impact of pests and dis- Deborah Golino. These two programs are part of the of Food and Agriculture eases on the state. Section 403 of the California Food National Clean Plant Network, and they work closely and Agriculture Code states that “the Department with CDFA’s nursery stock regulatory program to help [CDFA] shall prevent the introduction and spread of ensure that California fruit, nut, strawberry and grape injurious insects or animal pests, plant diseases, and nurseries have access to new varieties of pathogen- noxious weeds.” CDFA operates a pest prevention free propagative material to supply growers. system that includes pest exclusion, pest detection, CDFA Animal Health Branch (AHB) veterinar- pest eradication, public information and educa- ians provide the expertise in the detection of foreign tion, and pest identification and records. Its Plan for animal diseases and zoonotic diseases of concern. Pest Prevention complements UC’s EIPD Strategic Working with the UC ANR California Animal Health Initiative; it too focuses on exclusion of pests and and Food Safety (CAHFS) laboratory diagnosticians pathogens and rapid response to emerging problems. and researchers, they can provide a rapid detection Once pests become established, UC research and and diagnostic confirmation of livestock and poultry

100 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 It is estimated that the direct damage costs and the costs of controlling invasive species exceeds $138 billion per year in the United States. diseases. In the face of the exotic Newcastle disease outbreak in 2002 to 2003 in Southern California poultry farms, UC’s CAHFS developed a rapid assay, which reduced the time from sample submission to diagnosis from 5 to 7 days to 1 day and became the primary diagnostic tool to support the successful eradication Zhukova Elëna effort. fruit fly, palm weevils, polyphagous shot hole borer, foot and In 2012, USDA, CAHFS and AHB together provided person- mouth disease, BSE, avian influenza, exotic Newcastle disease, nel to assist in the investigation of a positive bovine spongi- anthrax, bovine tuberculosis, equine herpes myeloencephalopa- form encephalopathy (BSE) cow in the Central Valley. Part of thy, livestock toxicosis, bovine brucellosis and both land and the USDA National Animal Health Laboratory Network, the aquatic invasive plants. CAHFS lab is one of six labs in the United States that performs Integrated management of established invasive species. testing for BSE. CAHFS’s surveillance testing identified the Once a pest or pathogen becomes established, its ongoing man- initial inconclusive sample for BSE, which was then rushed to agement is a challenge for homeowners, land managers and the the National Veterinary Services Laboratory, where it was con- agricultural community, and methods must be developed to firmed to be positive. The investigation was crucial in isolating contain and control it. If it is a new pest or disease, this might the cow, confirming there was no risk to human or animal food require studying the biology of the organism, sampling tech- supplies, assuring foreign delegations that the U.S. safeguards niques, the natural enemies that control it in its country of origin for BSE are strong and ensuring the safety of the country’s beef and chemical controls (pheromones and pesticides). The UC products. The multibillion dollar U.S. beef export market was ANR network of research and extension personnel develop IPM preserved through these efforts. strategies that take into account effectiveness, sustainability, Rapid response to emerging problems. UC, using its sci- costs and impacts on the environment, and then communicate ence, outreach and research capabilities, can speedily and ef- them to a wide range of clientele, from large-scale commercial ficiently mount programs to tackle emerging threats from new growers and ranchers to homeowners. One form that the com- pests and diseases. For example, when the European grapevine munication takes is the UC IPM guidelines for California crops, moth (EGVM) was first detected in California in 2009, UC which provide monitoring methods and treatments that are cru- quickly developed degree-day models, lists of effective treat- cial for managing pests and diseases. In some cases, for example ments, and commodity-specific treatments for movement of the guidelines for managing Fuller rose beetle in citrus, these infested fruit and distributed that information and best man- guidelines provide best management practices that address phy- agement practices to growers and homeowners. Even as a threat tosanitary barriers enacted by foreign countries. is emerging, UC can provide provisional treatment CDFA has made strong contributions to the long-term man- guidelines until research can be conducted agement of pests and diseases through its grant programs. to provide science-based integrated pest The Specialty Crops Block Grant program offers grants management (IPM) recommendations. for projects that enhance the competitiveness of When quarantines and other California specialty crops. CDFA also has input on regulatory measures are deemed Farm Bill Section 10201 (Plant Pest and Disease necessary to help manage emerg- Management and Disaster Preparation) project ing pest and disease problems, funding priorities. UC ANR has a competitive UC scientific expertise and local grant program that funds research and exten- knowledge guide the regulatory sion programs from the Strategic Initiatives,

decisions made by CDFA. UC in- Zhukova Elëna including EIPD. These grant programs, in put is provided through USDA’s combination with other state and federal funds technical working groups, CDFA’s and commodity boards, support the univer- science advisory panels and ad sity’s excellent research and extension programs. hoc committees. UC and the regula- UC, through its research and extension pro- tory agencies have worked together on grams, and CDFA, through its diagnostics and regu- many cases of invasive pests and patho- latory activities, work together to address critical plant gens, including the Asian citrus psyllid/ and animal issues facing California. This special issue of huanglongbing complex, EGVM, diaprepes root California Agriculture highlights these and other collaborations weevil, light brown apple moth, red imported fire ant, glassy- and some of the successes of the many pest and disease pro- winged sharpshooter/Pierce’s disease complex, Mediterranean grams conducted in California. c

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 101 Research news Unwelcome arrivals alifornia’s numerous ports of entry and

borders provide plenty of opportunities ARS USDA C for exotic and invasive insects, weeds and plant diseases to enter the state. Some of these species are intentionally introduced, while others arrive accidentally. Once here, they can benefit from the lack of natural controls of their native environments and thrive in new plant or animal systems and management practices. Here are five significant and new arrivals to California under In July 2014, the investigation by UC scientists. USDA intercepted a shipment of giant African snails (shown scientists are asking the public above in an official’s to help prevent the spread of hand) in Los Angeles. this pest. Although the snails Polyphagous shot hole borer “If you have heavily infested haven’t reached the wild in California, In 2012, a South Gate (Los Angeles County) plant material, remove it, chip it UC researchers homeowner was searching the Internet to identify and cover it with a plastic tarp are working with mysterious symptoms in her backyard avocado tree. to get rid of the colony,” Eskalen scientists in Florida, She found Akif Eskalen, UC Cooperative Extension said. “Never move infested mate- where officials are trying to eradicate (UCCE) specialist in the Department of Plant rial to non-infested areas.” an infestation Pathology at UC Riverside, and emailed pictures. discovered in 2010. Giant African snail “As soon as I got the pictures, I realized it was something I had never seen before,” Eskalen said. When 68 giant African snails were intercepted at He visited the South Gate residence and identi- Los Angeles International Airport in July 2014, the fied the polyphagous shot hole borer, a tiny beetle news went viral. Gardeners, farmers and researchers from Asia that bores through bark carrying with it a were unnerved by a broadly circulated photo showing harmful fungus (Fusarium euwal- snails the size of grapefruits that had been seized in a lacea). The fungus attacks the shipment from Nigeria. tree’s vascular tissue, choking off Giant snails have a wide host range and feed vora- water, causing branch dieback ciously. Besides causing crop damage, the snails can and eventually killing the tree. transmit a parasitic nematode that can lead to menin- Polyphagous shot hole borer and gitis in humans. the fungus are now distributed The giant snails haven’t made it into the wild in widely in more than 110 types of California, but UC Riverside entomologist Jocelyn trees in Los Angeles and Orange Millar is working closely with scientists in Florida, counties, and have been observed where officials are trying to eradicate an infestation in San Bernardino, Riverside and discovered in 2010. Giant snails are difficult to root out San Diego counties. So far, in- because the small, newly hatched snails are hard to fested trees are mostly urban, but find, and when fully grown they are adept at hiding agriculturally important trees like in foliage and leaf litter. Millar, an expert on phero-

Gevork Arakelian, Los Angeles County Angeles Los Arakelian, Gevork olive and persimmon, as well as mone attractants, is looking for natural attractants avocado, are known hosts. that will draw them out of hiding and into traps. He UC Riverside scientists are researching control Eskalen is conducting research aimed at de- is working on the project with UC Riverside research measures for the feating the fungus, UC Riverside entomologist specialist Rory McDonnell, who is an expert on snail polyphagous shot hole Richard Stouthamer is researching the beetle’s and slug biology, and Amy Roda, a U.S. Department borer, an invasive beetle origin and UC Riverside entomologist Timothy of Agriculture Animal Plant Health Inspection from Asia that bores into trees and transmits a Paine is studying control measures for the beetle. Service (USDA APHIS) scientist specializing in pathogenic fungus. Until solutions to the problem can be found, the invasive species.

102 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 Quagga mussel “One thing in our favor is that surrounding lakes In 2010, officials were alarmed to learn that quagga are also uninfested,” Giusti said. “If quagga make it to mussel had invaded Lake Piru, a reservoir on the Shasta, Folsom or Berryessa lakes, we’re toast.” Ventura County–Los Angeles County border. A na- The most common way tive of Ukraine, the freshwater pest made its way to mussels are moved is rec- the U.S. Great Lakes in 1989. In 2007 they were found reational boating, but that’s “If quagga make it to Shasta, Folsom in Lake Mead and other lakes on the Colorado River. not the only threat. or Berryessa lakes, we’re toast.” At this time, it is not known how quagga reached For example, it is Lake Piru. It is the first appearance of the invasive common practice for fire- — Greg Giusti pest in a California water body that is not fed by the fighting agencies to dip Colorado River. equipment into lakes to collect water to fight fire. Quagga mussels multiply rapidly, encrusting boat Sabrina Drill, UCCE advisor for Los Angeles and hulls, engines and equipment, and clogging water Ventura counties, briefed firefighting officials about pipes up to two feet in diameter. They are voracious ways to prevent spreading the invasive species. filter feeders, clearing plankton from lakes that is “It might be OK to use water from Lake Piru to needed by native species. fight a fire in Lake Piru’s own watershed,” Drill said. “I shared best management practices for decontami- nating the equipment that was in contact with the in- Brown marmorated fested water — starting with making sure everything stink bug, a pest of is drained and completely dried before it is used in fruit and vegetable another lake.” crops, was first discovered in the Brown marmorated stink bug United States in Pennsylvania. “They’re here,” wrote UCCE advisor Chuck Ingels In California, in a September 2013 email to Sacramento growers. He reproducing populations have had just visited the midtown Sacramento site where been found in Los hundreds of brown marmorated stink bugs (BMSB; Angeles County and California Department of Boating and Waterways DepartmentCalifornia and of Boating Halyomorpha halys) were clustered Sacramento. together on a Chinese pistache street tree. Comments, emails and calls began pouring in. “These bugs were hor- rible when I lived in Pennsylvania,” commented Todd Jumper on the UC Agriculture and Natural Resources (ANR) website. “Hundreds of them in our home and (it was) literally almost Quagga mussels, native to Ukraine, impossible to stop them.” encrust boat Greg Giusti, UCCE advisor in BMSB is a pest of agricultural crops hulls, engines and Lake County, is working closely and a serious residential problem. It is equipment, and clog with county officials to a strong flyer and also travels long dis- water pipes. keep quagga mussels tances by hitching rides in vehicles or out of Clear Lake, inside furniture or other articles when the largest natural they are moved, often in late summer freshwater lake in and early fall. As a result, new infesta- California. Guisti tions pop up in neighborhoods where helped the county people travel from infested areas. draft an ordinance re- A native of China, Japan and Korea, quiring regular inspec- BMSB was first documented in the tions of boats launched United States in Pennsylvania in 2001. in Clear Lake. The local It is either established or found occa- media, the Internet, the sionally in about 41 states. D. Hamilton, CDFG Hamilton, D. California Department of Fish BMSB feeds on apples, pears, cher- and Wildlife and the vast fishing ries, peaches, corn, beans, tomatoes, community were part of an outreach effort to make berries and many other California people aware of the regulation. Failing to comply re- crops. Feeding creates pock marks

sults in a fine up to $1,000. and distortions that make the fruit Baldo Villegas

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 103 Research news

“In certain respects, [the come in from other countries, or it might have mutated here in California. There’s brown marmorated stink some suspicion viable downy mildew is car- bug] is one of the worst ried on seed, but the evidence at this point is invasive pests we’ve ever all circumstantial.” They do know an Imperial Valley grower had in California.” noticed bright yellow blotches staining spinach —Chuck Ingels leaves in 2012. It wasn’t long before samples were delivered to Koike, who operates UCCE’s only county-based plant diagnostic lab. “We have developed a very strong relation- ship with industry over the years,” Koike said. unmarketable. In grapes, “When growers start to see some breakdown berries collapse and rot in previously resistant varieties, they get in increases. Wine tasters touch with me.” The new race of have been able to detect Downy mildew will not grow in petri dishes, only downy mildew stink bug odor in wines Stephen Ausmus, on living tissue. Koike and his team washed the spores stains spinach leaves USDA ARS made from grapes that off the sample leaves and sprayed them onto 12 va- with bright yellow blotches. had as little as one bug per rieties of spinach in the lab. They assign a plus three clusters. or minus to each variety based on which “In certain respects, this is one of the worst inva- come down with the disease and sive pests we’ve ever had in California,” Ingels said. which stay healthy. In summer 2014, Ingels conducted a monitoring “This creates a finger- program for BMSB in Sacramento County funded print of the pathogen,” by the California Pear Advisory Board and the Lodi Koike said. “We match Winegrape Commission. Ingels said his team docu- the fingerprint to see if mented the population fluctuations of BMSB in mid- it is a known race. In town Sacramento. He found no bugs in traps near this case, it was a brand farms south of Sacramento along the Sacramento new fingerprint, so we River. UCCE advisors Lucia Varela and Rachel Elkins, realized we likely had a also with funding from the Pear Advisory Board, new race.” conducted BMSB monitoring programs in Lake and Mendocino counties; none were found. “They don’t seem to be spreading fast,” Ingels said. “When growers start to see some “We’ve learned that it takes four or five years for a breakdown in previously resistant major reproducing population to build up. That sug- varieties, they get in touch with me.” gests they could be on farms, but we haven’t found them yet.” —Steven Koike In the meantime, problems persist in midtown Sacramento. The same test was conducted by “Restaurants are concerned that the stink bugs are James Correll, a plant pathologist at visible on the walls and crawling on tables. A couple the University of Arkansas and Koike’s of apartment managers called me to say their tenants frequent collaborator, who reached the are threatening to move out if they are not controlled,” same conclusion. In 2014, the International Ingels said. “They are a nuisance, so they are already Working Group on Peronospora farinosa having an economic impact.” (IWGP) in The Netherlands designated Koike and Correll’s isolate as race Pfs: 15. Downy mildew The IWGP promotes consistent and clear com- In the plant disease world, the introduction of new munication between public and private entities — sci- pests is more ambiguous than with insects. In Imperial entists, farmers, plant breeders and others — about all County, for example, farmers are dealing with a new resistance-breaking races that affect a wide area and

race of downy mildew in spinach (Peronospora farinosa cause significant economic impact. Koike and Correll’s Koike T. Steven f. sp. spinaciae). work contributed to this international effort. c “We don’t know where it may have come from,” —Jeannette Warnert said Steven Koike, UCCE plant pathologist for Monterey and Santa Cruz counties. “It could have

104 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 OngoingOutlook research A look at EIPD Strategic Initiative projects

ANR‘s five strategic initiatives seek new ways of partnering within and outside the university to tackle emerging issues in California. As UCpart of this strategic vision, the Division annually funds research and extension projects in and across all initiatives. Four recent and ongoing studies in the Endemic and Invasive Pests and Diseases Strategic Initiative are profiled here. Tatiana Roubtsova Tatiana Thousand cankers disease

housand cankers disease “is a rapidly emerging the beetle, the genetic Tinvasive threat to walnut orchards in Califor- diversity of the fun-

nia,” says Richard Bostock, plant pathologist at UC gus and the biology Seybold and Steve Stacy Hishinuma Davis and a lead researcher on a 3-year study of the of the beetle. The disease. “Only in a few places in the state have Eng- disease appears to be lish walnut trees died due solely to this disease,” he present in all areas; in Top, culture of says, “but it’s on its way to becoming endemic in all some orchards, there Geosmithia morbida, the fungal pathogen the walnut-growing areas, and we are still not sure is a very low inci- that causes thousand cankers where this is going to go.” dence of the disease, disease. Middle, close-up of The fungal pathogen, while in others, as walnut twig beetles tunneling Geosmithia morbida in the bark of an infected tree. , was new to many as 90% of the Bottom, actual size of the beetle science when it was found in trees have WTB at- in relation to a penny. Stacy Hishinuma California in 2008 in Northern tacks and cankers. California black walnut trees Thousand cankers disease has decimated growing in Davis. Its vector, eastern black walnut, Juglans nigra, in landscape the walnut twig beetle (WTB), and urban plantings in some Western states and has been known in California parts of Colorado, where, in 2008, the association since 1959. The male beetles of the beetle and fungal pathogen in the disease attack a tree first, releasing a was first discovered and reported by researchers pheromone that attracts thou- at Colorado State University. In 2010, the disease sands of beetles to the phloem was reported on eastern black walnut in Tennessee tissue of the and subsequently in other Eastern states within tree’s trunk the native range of this species. In California, the and large research team has documented the disease in the branches, Southern California black walnut, Juglans californica, where they in English walnut, Juglans regia, which is the com- tunnel, feed mercial orchard species, and in Northern California and produce black walnut, Juglans hindsii, which is used as a Above, a heavily infected offspring. rootstock for J. regia, and also in Paradox rootstocks. Southern California black walnut (Juglans Spores of the “About 70% of commercial trees are on Paradox,” californica) showing sap- pathogen says Bostock, and the study has discovered that staining of the bark and Bostock Richard are carried “Paradox is highly susceptible and is very attractive dieback. Inset, a canker underneath the outer on the vec- to the beetles.” Investigating the population struc- bark of a Paradox hybrid tor’s body and infect the host tissue; the cankers ture of the fungus in different geographic regions in walnut showing necrosis produced by the pathogen coalesce and can girdle the United States, other researchers have reported around walnut twig beetle a trunk or branch, and in severe cases can cause de- “a great deal of diversity in the fungal popula- tunnels. cline and death of the tree. tion in Arizona, California and New Mexico,” says The study, reaching completion now and co- Bostock, “and their findings suggest that these states directed by Steven Seybold, a USDA Forest Service could be the source of the thousand cankers disease entomologist, has assessed the distribution of thou- epidemic.” sand cankers disease in the state’s walnut-growing The susceptibility of Paradox and the destruction areas, differences among walnut (Juglans) species in the disease has caused in eastern black walnut are their reaction to the pathogen and attractiveness to cause for concern, but “we are not raising a lot of

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 105 Ongoing research

alarm bells at this point,” says Bostock. Researchers Entirely unknown is why thousand cankers disease suspect thousand cankers disease may be contributing apparently emerged recently in California and spread to the complex of diseases, including Phytophthora so fast. The beetle has been reported in the state for root and crown rot, lethal Paradox canker and crown decades but has not been considered a significant pest; gall, that cause decline in walnut trees. Thousand can- however, this insect–pathogen association presents kers disease has been found in the stems of even very a new challenge for growers, whose 2013 crop was young vigorous English walnut trees, and yet it seems valued at nearly $1.8 billion according to the USDA the trees can grow out of it. However, when it begins National Agricultural Statistics Service. “Something in the crowns of older trees and progresses down- has changed with these beetles and their association ward, it is often fatal. with this pathogen that has led to the widespread

Elizabeth Fichtner Elizabeth The current suggested treatment for severely dis- occurrence of the disease we are now seeing in the Characteristic entry and eased trees is removal and burning on site, if burning state,” says Bostock. exit holes of the walnut is allowed. Study team members Elizabeth Fichtner The research team also included Mohammad Yaghmour twig beetle in the trunk of (UCCE Tulare County) and Seybold have found that (Plant Pathology, UC Davis), Stacy Hishinuma an English walnut tree in Tulare County. The holes the majority of WTBs begin to emerge from infested (Entomology, UC Davis), Tivonne Nguyen (Plant are less than 1 millimeter wood by late spring, suggesting that tree removal Pathology, UC Davis), Tatiana Roubtsova (Plant Pathology, in diameter. and sanitation should be conducted by March, or UC Davis), Carolyn DeBuse (USDA-ARS), Mary Louise April at the latest. The beetles fly nearly year-round Flint (UC IPM), Janine Hasey (UCCE Sutter-Yuba coun- in California, but the primary flights are in May/June ties) and Richard Hoenisch (Plant Pathology, UC Davis). and September/October.

Asian citrus psyllid and huanglongbing disease he bacterial pathogen that causes the citrus disease infected with the pathogen have been found, “but the Thuanglongbing (HLB) is on its way to California; trees are not showing infection yet.” it is vectored by the Asian citrus psyllid (ACP), which The project team’s goals have been to create and is established in Southern California keep up to date a “one-stop” online information hub and has moved into citrus orchards in that provides California growers and homeowners the Central Valley. “There is currently with what they need to know to help delay the arrival no cure for this disease,” explains Beth of HLB. In the first year of the project, 2012, the team Grafton-Cardwell, UCCE specialist and set up the ACP/HLB Distribution and Management research entomologist at UC Riverside website, ucanr.edu/sites/acp/. This site provides us- and lead researcher on a 5-year project ers with a Google map to locate their property in rela- to alert and prepare growers and the tion to the reported findings of ACP, HLB and releases public. “HLB kills citrus trees, and it’s of the biological control wasp Tamarixia. They are also spreading northward from Mexico provided guidelines on how to protect their trees. fast,” she says. The map currently shows a single red circle in The symptoms of HLB are progres- Los Angeles, which signifies the only documented sive mottling of leaves, deformed instance to date of HLB in California. It was recorded and off-flavor fruit, plant stunting in 2012 in an urban backyard citrus tree. That inci- and eventual plant death. HLB was dence of the disease “was eliminated,” says Grafton- first identified in Florida in 2005, and Cardwell, “but we are afraid HLB will turn up citrus acreage and fruit yields in that somewhere again soon.” state have dropped precipitously since Most of the California catches of ACP, plotted by Elizabeth Grafton-Cardwell Elizabeth then, according to Grafton-Cardwell. square mile on the website map, are in urban back- Symptoms of ACP spreads the disease quickly; the yard trees in Southern California. It’s estimated that huanglongbing disease, nymphs of the insect can feed on infected tissue after 60% of Californians have a citrus also known as citrus greening, include mottling they hatch and carry the disease to other tree. Statewide, the number of of leaves and greening trees when they emerge as adults. “ACP citrus trees in residential gardens of fruit. is a very efficient vector, so not many exceeds the number in commercial psyllids are needed to spread the dis- orchards. The website ease,” says Grafton-Cardwell. And yet, gives homeowners the disease symptoms don’t show information on iden- up in the trees for 1 to 2 years after tifying the psyllid, infection, by which time infection has already spread. In some areas of Texas, she says, “hot psyllids” Adult Asian citrus psyllids (actual size).

106 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 Michael E. Rogers Michael E. Rogers

and directions on what to do if an ACP is found: Act and retail nurseries. The team fast! Call the California Department of Food and works with local grower task Agriculture (CDFA) hotline, 1-800-491-1899, to re- forces in citrus areas infested port the finding; if it’s a finding in a new area, CDFA with ACP, such as the Imperial provides eradication treatment, but if ACP is already Valley, Ventura County and Top, Asian citrus psyllid adult and nymphs. established in the area, the homeowner is directed to the San Joaquin Valley, helping Middle, adult psyllid on finger at actual size. manage the psyllids on their own. them to develop ACP manage- Bottom, nymphs tucked down in new leaves. Economist Karen Jetter (Agricultural Issues Center, ment strategies. The website UC Davis) has created tables on the website showing is used as an educational tool the costs of various treatments for both homeowners during these meetings. Grafton- and growers. A cost calculator helps conventional and Cardwell communicates a clear message that insec- organic growers compare the cost per acre of various ticide spraying to slow the spread of ACP and keep chemical options. “We are in the process of surveying numbers low is critical for preventing psyllids from growers in various regions of the state to determine finding diseased trees and helps to buy time for re- what chemical choices they have made over the last 4 searchers to develop a cure for the disease. years, so that we can provide an analysis of costs by Other members of the project team are Matthew region,” says Grafton-Cardwell. Daugherty (Entomology, UC Riverside) and Robert Johnson For outreach, the project team is providing train- (UC ANR Informatics and GIS Program). ing to the general public through Master Gardeners Elizabeth Grafton-Cardwell: Above and fingertip

Bovine respiratory disease ovine respiratory disease is one of the leading A survey questionnaire was sent to 1,450 dairies Bcauses of death in preweaned dairy heifers in the in 2012 with questions on calf management practices. United States. To help dairy farmers diagnose and The data was statistically analyzed to identify the control the disease, a new scoring system to assess the most important factors that may be related to the risk respiratory health of preweaned dairy calves has been of bovine respiratory disease. Then, a model-based developed in research led by Sharif Aly at the Vet- scoring system was developed for six clinical signs: erinary Medicine Teaching and Research Center, UC eye discharge (2), nasal discharge (4), ear droop or Davis. Called the California Bovine Respiratory Dis- head tilt (5), spontaneous ease Scoring System, it is composed of six questions cough (2), rapid or diffi- requiring only yes/no answers and can be easily used cult breathing compared on-farm by owners, veterinarians and farmworkers. to other calves (2) and The 4-year study began in 2012. The goals of the temperature at or above research were to collect data on current management 102.5°F (2). A score of 5 practices and to develop a simple, low-cost clinical or higher suggests a calf diagnostic scoring system that could be used on farms may have respiratory to identify clinical signs early, avoid unnecessary ani- disease. mal deaths and misuse of antimicrobials, and track the The scoring system health of calves over time. has been validated in a study of 500 calves on three dairy farms and two calf ranches in California; results are expected to be published in 2015. One of the ad- The California Bovine vantages of the California scoring system compared Respiratory Disease

Dairy Epidemiology Lab, UC Davis Dairy Epidemiology Lab, to the Wisconsin scoring system, developed in 2008, Scoring System allows owners, vets is that it requires less calf handling and allows easier and farmworkers assessment of clinical signs. A recent study compared to easily diagnose the diagnoses of both systems and showed excellent respiratory disease agreement beyond chance. in preweaned calves. Aly stresses how easy it is to use the California scoring system. “We’ve had very good feedback from dairies,” he says. “Assessing each clinical sign as pres- ent or absent takes the guesswork out of diagnosis. In addition, the scores and cut-off for case status are

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 107 Ongoing research

model based.” Because it is so simple, the scoring sys- different dairies for the risk of bovine respiratory dis- tem can be used daily, for example, on sick calves to ease in collaboration with dairy farm advisors and UC confirm respiratory disease status prior to treatment. Cooperative Extension specialists. The team’s current research is focused on develop- The research team also includes Terry Lehenbauer and ing a risk assessment tool that incorporates the new Alison Van Eenennaam (Animal Science, UC Davis), scoring system and also a questionnaire, based on Randall Anderson (CDFA), Alejandro Castillo (UCCE the statewide survey, that points to risk mitigation Merced County), Carol Collar (UCCE Kings County), strategies. The questionnaire can be completed by a Christiana Drake (Statistics, UC Davis), Jennifer Heguy calf raiser and the herd veterinarian to form a disease (UCCE Stanislaus County), Lindsey Hulbert (Animal control plan. The scoring system can be used to moni- Science, UC Davis), Betsy Karle (UCCE Glenn County), tor the prevalence of respiratory disease in calves Frank Mitloehner (Animal Science, UC Davis), Nyles once control measures are implemented. The risk as- Peterson (UCCE San Bernadino County) and Noelia Silva- sessment tool will be used to monitor 5,000 calves on del-Rio (UCCE Tulare County).

Pest and disease risks in compostable wastes alifornia municipal waste plans and air mulch, which can allow a pest or disease to be easily Cquality regulations are shifting green waste spread by wind, water or wildlife. processing from composting operations, Crohn, who is a waste management specialist, and where materials must be heated to at a team of other UC specialists, farm advisors and grad- least 122°F, at which few pathogens uate students set up simulated composting and chip survive, to chip and grind opera- and grind environments and compared the survival tions, where pile temperatures may rates of Asian citrus psyllid, citrus leafminer larvae, not exceed 122°F. “The question,” says tobacco mosaic virus, fusarium in palms, bermudag- David Crohn, associate professor of rass, nutsedge, and clover and tomato seeds. In each environmental science, UC Riverside, environment, pest and disease samples were either “is whether there’s a potential for placed in mesh bags or in envelopes in the green waste pests and diseases, such as the material, and either the material was heated to 122°F Asian citrus psyllid, to survive (i.e., composted) or kept at 77°F, ambient temperature, chipping and grinding and be for 3 days. spread to disparate locations.” “The results were a mix,” says Crohn. “Citrus The preliminary results of a leafminer was controlled by chipping and grinding; recent research project suggest there is that risk. Asian citrus psyllid, though, had some survival in

David Crohn David Assembly Bill 341, passed in 2012, required state chipping and grinding but was controlled by compost- government to plan for 75% of municipal waste to be ing.” In terms of the weeds, chipping and grinding A UC study found diverted from landfills by 2020. This will be possible “was effective at inactivating nutsedge, but clover and that some insects only if millions of tons of green waste are recycled. As tomato seed survived it just fine.” and weeds survived grinding (left) and stricter environmental regulations increase the cost Crohn stresses this was a small study, and it is im- chipping (right) of opening and operating compost operations, more possible to simulate the variety of conditions in com- operations. green waste will be going to chip and grind opera- mercial green waste operations. But in terms of the tions; and the resulting material can be moved out of risks of invasive pests and diseases being spread more the facilities within a few days, transported over some- easily and rapidly through chipping and grinding, the times long distances and applied in diverse locations: preliminary results, he says, “suggest there’s reason orchards, parks, gardens, farms, commercial land- for concern.” scapes and roadsides. It is usually applied as a surface The next step of the research is to analyze the economic impact of the state regulatory policies on composting and chip and grind operations. Chip and grind operations are exempt from costly new rules to protect air and water quality; composting facilities are not exempt. The project team also includes Matthew Daugherty (Entomology, UC Riverside), James Downer and Ben Faber (UCCE Ventura County), Deborah Matthews (Plant Pathology, UC Riverside) and Steven Swain (UCCE Marin County). c Cassandra Cannon, CDFA Cannon, Cassandra Grafton-Cardwell Elizabeth —Hazel White Asian citrus psyllid nymphs (left) and citrus leafminer damage (right).

108 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 EXCLUDING PESTS AND PATHOGENS he optimal way to control new biological threats to agriculture, natural resources, communities and human health Tis to prevent them from arriving in the first place. If detected and intercepted early enough, a pest or disease may be eradicated completely. This ability to quickly detect and identify a new arrival depends on having diagnostic expertise, infrastructure and resources in place. The articles in this section highlight UC’s work and partnerships in this critical stage of protecting livestock and plant systems.

Diagnostics in animal health: How UC helps exclude and minimize impact of livestock pathogens by John M. Adaska, Edward R. Atwill and Glenn A. Nader

UC has a wide reach in the agriculture sector of the California economy and is well ash receipts for California’s total recognized for research expertise in plant diseases. Less well known is the role UC plays livestock and livestock products were $12.3 billion in 2011 (table 1). in animal agriculture. In 2012, the California Animal Health and Food Safety lab at UC C The responsibility for protecting the live- Davis performed nearly 980,000 tests on samples from sick livestock, including cattle, stock industries and, by extension, food horses, pigs, chickens and turkeys. The lab is prepared to respond rapidly to any disease safety and security, in the state falls on an outbreak or identification of a foreign disease. Researchers at the School of Veterinary integrated system that starts on the farm and extends to a wide array of private Medicine at UC Davis are testing novel subunit vaccines to prevent pinkeye in cattle; UC and public entities. UC has a large role ANR specialists and advisors and the staff at the Sierra Foothill Research and Extension in outreach, education, surveillance and Center were key to the development of best management practices that landowners response to significant animal disease and resource managers are using to protect their herds and public water sources events, and faculty and staff at each of the UC campuses are involved. against the parasite Cryptosporidium parvum; and UC veterinary scientists are part of a large team of experts, including state and federal agencies, determined to combat the The CAHFS laboratory system endemic bluetongue virus, which can affect the state’s exports. The California Animal Health and Food Safety (CAHFS) laboratory system is funded in large part by the California Department of Food and Agriculture (CDFA) and operates within the UC Davis School of Veterinary Medicine (SVM). CAHFS is the backbone of California’s early warning system to safeguard public health from foodborne pathogens, toxins and diseases common to animals and hu- mans. CAHFS also protects the health of California’s livestock and poultry popula- tions by providing broad-based surveil- lance for all catastrophic animal diseases not currently found in the United States (referred to as foreign animal diseases, or FADs). CAHFS must immediately detect an introduction of a highly contagious disease like avian influenza in poultry and foot and mouth disease in livestock to minimize the devastating effects it would inflict on consumer confidence and California’s agricultural economy. As a result, CAHFS is responsible for the vast

Elëna Zhukova Elëna Online: http://californiaagriculture.ucanr.edu/ UC campuses and UC Cooperative Extension work with the CAHFS lab system, funded largely by CDFA, landingpage.cfm?article=ca.v068n04p109&fulltext=yes to research livestock diseases, protect animal health and respond to disease outbreaks. doi: 10.3733/ca.v068n04p109

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 109 TABLE 1. California livestock, dairy, poultry and apiary income, 2010 and 2011 majority of diagnostic testing of livestock samples within the state. In 2012, the lab 2010 2011 Change system had 30,567 cases submitted to it ...... $1,000s ...... % (4,255 equine, 6,952 bovine, 1,855 caprine, Aquaculture 58,200 64,036 10 340 porcine, 819 ovine, 2,064 other mam- Chickens, all 721,724 702,051 –3 mals, 3,063 chicken, 477 turkey, 1,114 other Cattle and calves 2,068,412 2,825,125 37 avian, and 9,805 cases in which a species was not provided, involving feed or bed- Eggs, chicken 367,788 391,578 7 ding samples, etc.) and performed nearly Hogs and pigs 36,063 39,196 9 980,000 tests. The case load that year Honey 42,579 28,594 –33 included over 10,800 necropsies (animal Milk and cream 5,928,150 7,680,566 30 autopsies) of whole animals or animal Sheep and lambs 66,060 NA NA tissues submitted for full diagnostic work- Turkeys 262,910 287,463 9 up (E. Sanson-Smith, CAHFS, personal Wool and mohair 3,835 5,050 32 communication). The work-ups typically Other livestock 218,617 269,345 23 include post-mortem and microscopic Total 9,819,519 12,357,994 26 examination, bacterial cultures, testing for Source: USDA NASS 2012. viral infections, testing for antibody levels and, in some cases, testing for the pres- ence of toxic agents. CAHFS is a member of a number of Chicken or important national diagnostic networks, cow gets sick. including the National Animal Health Laboratory Network (NAHLN) (h t t p s :// www.nahln.org) and the Food Emergency Response Network (FERN) (fernlab.org/). NAHLN is a partnership of federal, uni- versity and state veterinary diagnostic Animal dies. laboratories across the United States and Owner or vet is a surveillance and emergency response takes a sample system that provides critical and ongo- (blood, urine, Owner or vet brings carcass to CAHFS. ing resources for disease surveillance feed, etc.) and sends to testing, information management, qual- ity assurance and the development and Necropsy (animal autopsy) is performed. CAHFS. Samples are taken by pathologist. validation of new diagnostic tests. FERN is also a federal-state partnership and provides critical and ongoing resources for responding to microbiological, chemi- cal or radiological food contamination Depending on animal type, history of problems, environmental conditions incidents, for which the U.S. Department and symptoms, testing is assigned. of Agriculture (USDA) and the U.S. Food and Drug Administration (FDA) have regulatory authority. Bacteriology, virology, toxicology, molecular, EM, immunology and/or histology testing is performed. How samples get to the labs The primary route by which samples get to CAHFS labs is through submis- Case coordinator uses test results to determine diagnosis. sions by private veterinarians, owners and state and federal regulatory authori- ties (fig. 1). This widely diverse group of Diagnosis is sent to client. people ensures that the surveillance is broad based from both geographical and industry perspectives. The laboratory sys- tem has four locations in the state: Davis, Client can make changes to prevent future reoccurrance of disease. Turlock, Tulare and San Bernardino

Photos: chicken, Mike Poe; calf, Elëna Zhukova Elëna calf, Mike chicken, Poe; Photos: (cahfs.ucdavis.edu/). The Davis laboratory is adjacent to Fig. 1. The route that samples from a diseased animal and the subsequent case follow through the the SVM complex on campus and is California Animal Health and Food Safety (CAHFS) laboratory system. the largest of the four laboratories. The

110 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 Research into livestock diseases Research conducted within UC, in- cluding the Agriculture and Natural

kakisky / MorgueFile Resources (ANR) network of advisors, specialists, and UC Davis College of Agricultural and Environmental Sciences (AES) faculty and the staff at the many ANR Research and Extension Centers (RECs), is vitally important in helping the state’s producers control endemic diseases of livestock, safeguard the microbiological safety of food and water and improve the sustainability of production agriculture. Pinkeye. One disease that affects both beef and dairy cattle statewide is pinkeye, also known as infectious bovine kera- toconjunctivitis (IBK). IBK is the most common eye disease of cattle worldwide (Angelos 2009). Compared to human pinkeye, bovine pinkeye is a much more devastating disease as it affects not only the conjunctiva surrounding the eye but also the cornea itself, and in severe cases causes blindness following rupture of The CAHFS lab in San Bernardino was instrumental in the diagnosis and eradication efforts during the 2002–2003 outbreak of exotic Newcastle disease, which was originally diagnosed in a backyard chicken. the eye. IBK is a multifactorial disease, meaning that many different factors Davis lab receives a variety of avian and tuberculosis) in a small number of dairy contribute to its development, including mammalian livestock samples for diag- herds in California. environmental conditions (plant awns nostic evaluation and is the site for both The San Bernardino lab also works such as foxtails, dust, ultraviolet light), in- the CAHFS toxicology section and the with both mammalian and avian species sects (flies), bacteria Moraxella( bovis) and equine drug testing program. The toxi- and was instrumental in the diagnosis viruses (Angelos 2009). cology section is nationally recognized and eradication efforts directed at the Dr. John Angelos, an SVM professor, and has partnerships with a variety of exotic Newcastle disease (END) outbreak is building on the earlier work by Lisle federal agencies, such as the Federal in 2002 to 2003 in Southern California George (retired) in conducting research Bureau of Investigation (FBI), the FDA, (Nolen 2002). The original diagnosis of into the pathogenesis and prevention of and the Centers for Disease Control and this economically important disease this important disease. Their collective Prevention (CDC). Faculty and staff in was made on a backyard chicken that work has helped characterize impor- this section routinely test for toxins such had been referred to the San Bernardino tant pathogenic factors associated with as oleandrin and various rodenticides as lab by a local small-animal practitioner. Moraxella bovis and identified genes en- well as natural substances such as nitrate, Eventually the effort to control and eradi- coding these factors (Angelos et al. 2001; copper and lead. cate this disease from California involved Angelos, Ball et al. 2007). In addition, The Turlock laboratory performs test- nearly 1,700 personnel from numerous they have discovered Moraxella bovoculi, ing on avian samples and was instrumen- agencies and a total cost to tal in the identification of very virulent the state and federal govern- infectious bursal disease (vvIBD) in the ments of $168 million over

state in December 2008. This disease, by 10 months (E. Sanson-Smith, Angelos J.A. infecting an organ important in the im- CAHFS, personal commu- mune response in commercial poultry, nication). The CAHFS San can cause severe morbidity and mortality. Bernardino branch served The disease has been present in Europe as the central entry point for for a number of years but, until it was rec- birds that were necropsied ognized by the diagnosticians in Turlock, on-site and for samples that had not been reported previously in the were shipped to the USDA United States (Pitesky et al. 2013). National Veterinary Services The Tulare lab works with both mam- Laboratory and the Davis malian and avian species and has had CAHFS lab for testing for the a significant role in recent identifica- presence of the causal virus. Bovine pinkeye, the most common eye disease of cattle tion and eradication efforts directed worldwide, affects not only the conjunctiva surrounding the eye, toward Mycobacterium bovis (bovine but also the cornea itself, and in severe cases causes blindness.

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 111 another Moraxella species believed to play parvum. Following several community The research team conducted a series a role in bovine pinkeye (Angelos, Spinks outbreaks of this disease in the 1990s, of epidemiological studies in livestock et al. 2007). Current research efforts are concerns escalated by regulatory agencies herds on the risk factors for animal directed at developing and testing novel and drinking water districts that livestock infection and also DNA fingerprint- subunit vaccines as well as testing alter- were loading watersheds with this para- ing projects to investigate which spe- nate routes of vaccination such as intra- site resulted in ad hoc grazing restrictions cies of Cryptosporidium were being shed nasal vaccines to prevent IBK (Angelos on private and public rangeland water- by wildlife and livestock and whether et al. 2010, 2012). Collaborative efforts sheds (Atwill et al. 2012). To clarify the these strains were infective for humans between SVM and UC Davis Department processes causing this emerging human (Rochelle et al. 1999; Xiao et al. 2002). of Animal Science faculty and UC health risk and to develop practical farm- Perhaps more importantly, the team con- Cooperative Extension (UCCE) person- level solutions for the state’s livestock ducted a series of experimental soil box nel and ANR resources such as the Sierra industry, a large collaborative effort was trials at the Veterinary Medicine Teaching Foothill Research and Extension Center initiated in the late 1990s by ANR special- and Research Center, SVM, followed (SFREC) have greatly enhanced research ists, advisors and faculty at UC Davis. Key up by a set of detailed field trials at the into the pathogenesis and prevention of members of the collaboration included SFREC and the San Joaquin Experimental IBK under naturally occurring conditions Rob Atwill, SVM; Ken Tate, Thomas Range, USDA Forest Service, that studied typical for California’s cattle industries. Harter and Randy Dahlgren, AES; UCCE the efficacy of vegetative buffers to re- Cryptosporidium parvum. One of the advisors and their staff throughout move waterborne pathogens from range- leading waterborne infectious diseases California (e.g., livestock and natural re- land runoff (Atwill et al. 2002). that is transmitted between animals and sources, watershed, and dairy specialists); The collaborations on this disease humans throughout the United States is state and federal agencies; local water research have created one of the largest the protozoal parasite Cryptosporidium districts; private landowners; and live- and most integrated scientific teams in stock and agricultural organizations such the United States working on waterborne as Backcountry Horsemen of California, pathogens in agricultural watersheds. California Cattlemen’s Association and The results are a variety of practical and the California Wool Growers Association. adoptable best management practices and science-based tools that livestock owners and resource managers can use to reduce the risk of waterborne patho- Left, photomicrograph of Cryptosporidium gens from livestock grazing (Atwill et parvum oocyst at 10,000× magnification. Below, Lake Kaweah in the Sierra foothills of California, al. 1999). The efforts of ANR, ranging one of the watersheds in which researchers from the specialists and advisors to the studied comanagement of livestock grazing and staff and resources at the SFREC, were

Edward R. Atwill Edward water quality. key to the development of these best management practices, which are widely adopted today by both landowners and resource managers. Bluetongue. Bluetongue (BT) is a non- zoonotic disease of certain wild and do- mestic species of cloven-hoofed ungulates with substantial adverse economic impact on livestock production in California. The causative agent of BT, bluetongue virus (BTV), is an arbovirus that is spread through temperate and tropical regions of the world by biting Culicoides midges, which serve as biological vectors. There are several different serotypes of the BTV, and the individual serotypes may be en- demic or newly introduced; the newly in- troduced serotypes often cause outbreaks of disease in naïve animals. The global distribution of BTV infec- tion has recently altered, likely driven in part by climatic influences on the midge vectors resident in different regions. Similarly, the behavior of BTV infection of livestock has recently altered, with

John M. Adaska an alarming apparent increase in the

112 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 Elëna Zhukova Elëna Scott Bauer, USDA ARS USDA Scott Bauer,

The global distribution of Bluetongue disease, an arbovirus that affects sheep, cattle and othercloven-hoofed ungulates, is spread by a biting midge (Culicoides sonorensis) and is an ongoing cause of economic loss to BTV infection has recently livestock producers in California. UC researchers are part of a collaborative effort to conduct bluetongue virus infection prevalence studies and to develop predictive models. Left, a 1⁄16 inch altered, likely driven in part long, female, biting midge. by climatic influences on the midge vectors resident in studies for the predictive modeling of this education and applied research with emerging and economically important livestock producers in both the manage- different regions. arboviral infection. ment of endemic diseases and in the The group’s specific objectives are to surveillance for foreign animal diseases. perform spatial BTV infection prevalence They are supported by three statewide occurrence of overt disease in infected studies to identify environmental, cli- veterinarian specialists, who provide a cattle (MacLachlan and Mayo 2013). BTV matic and land-use (and anthropogenic) conduit for information from the campus has long been endemic in California and characteristics associated with regional to livestock producers. This network of is an ongoing cause of economic loss to (local-scale) BTV infection rates of live- advisors and specialists also provides livestock producers, with both direct stock in different regions of California. identification of diseases occurring in the losses caused by reduced production of Initial studies were focused on intensively field based on observed clinical signs. The infected animals and, even more impor- farmed dairy cattle, and the group is ex- CAHFS laboratory system then confirms tantly, the adverse impact of nontariff panding its investigations to free-ranging these observations with laboratory find- trade restrictions, which close lucrative cattle and sheep. The studies also include ings. The link provided by UCCE person- potential export markets. extensive entomological investigations to nel between producers and CAHFS is Researchers within the UC system better define the impact of climatic and also used to inform producers about any target bluetongue in a collaborative ef- anthropogenic drivers of the population new diseases in their area. UCCE works fort involving individuals at SVM, UCCE, dynamics of vector midges, and their with producers and their veterinarians UC Riverside, CDFA, CAHFS, USDA, and subsequent impact on the dynamics of on management actions they can take to also local veterinarians and local cattle BTV infection. Lastly, the group is study- minimize the occurrence of the disease in and sheep producers. These extensive ing the feeding behaviors of the vector their herd. Applied research may also be interactions and collaborations are critical midge species that might be important required with laboratory analysis to de- to the intensive surveillance studies that virus vectors in California and genetically termine the effectiveness of the mitigating underpin ongoing efforts to develop accu- characterizing the evolution of the types management action. rate and predictive mathematical models of BTVs that circulate in the state, includ- Recently, the CAHFS laboratory relevant to this economically important ing, most recently, a newly incursive novel database of toxicological findings was arboviral disease of livestock. The re- virus serotype. mined for use in a UCCE publication on search group, led by Dr. Jim MacLachlan, poisonous plants in California (Forero Outreach to producers has an extramurally funded (currently by et al. 2011). It reported that for all kinds NIFA USDA) project to further character- UCCE has 23 livestock advisors spread of livestock the number one reported ize the ecological drivers of BTV infection across the state (ucanr.edu/sites/UCCE_ problem from toxic plants was olean- among Culicoides vectors and ruminant LR/Beef_Cattle/Beef_Cattle_Advisors/). der, with over 555 cases during 17 years hosts in the state. The long-term objec- They play an important part in the ani- (fig. 2). Although this plant is used by tive is to utilize data generated by the mal disease network, serving a role in Continued on page 116

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 113 Elëna Zhukova Elëna Solving the puzzle of foothill abortion in beef cattle

by Glenn A. Nader, Mike N. Oliver, Julie A. Finzel, Myra T. Blanchard and Jeff L. Stott

oothill abortion, also known as epizootic bovine abortion (EBA), and through the 1970s, chlamydia was considered as a possible Fhas been a long-standing problem for California beef cattle causative agent. During this period, a field trial was conducted with producers. It is a major source of economic loss for California cow cooperator cattle in Lassen County in which susceptible heifers and calf producers, and in the 1990s it was estimated that 5% to 10% were fed tetracycline crumbles, and the data suggested there might (45,000 to 90,000 calves) of the California beef calf crop may be lost be some protection from the antibiotics. Numerous chlamydia each year (Bushnell et al. 1991). UC Cooperative Extension (UCCE) vaccines were prepared and given to susceptible heifers, but this farm advisors, specialists and UC Davis School of Veterinary Medi- effort was ultimately abandoned when heifers continued to abort cine (SVM) faculty have worked on this disease for nearly 50 years. following vaccination. This long research process finally moved forward in 2005, when the In the 1970s and early 1980s, viruses were considered as possible causative agent was identified. causative agents. A large research effort was initiated, with over 80 The Pajaroello (pa-ha-WAY-lo) tick, Ornithodoros coriaceus, is viruses isolated from the tick. After exhaustive work, research on responsible for transmitting the causative agent (a deltaproteo- causative agents moved from viruses to spirochete-like organisms; bacterium) when it feeds on a pregnant cow. The Pajaroello is a a Borrelia species was suggested to be a potential cause of EBA, but soft-bodied tick that resides in dirt or litter under trees and bushes, further experimental studies essentially eliminated spirochetes and locations where deer and cattle typically bed down. The Pajaroello Borrelia species as potential causative agents. does not embed itself in animal flesh, but rather it feeds rapidly (for With no definitive causal agent of EBA identified, the California as little as 20 minutes) and then drops back onto the ground. It Cattlemen’s Association gave UCCE a grant from its Livestock can survive for years in a dormant state, without taking a Memorial Research Fund to develop educational outreach blood meal. through a video on how to manage cattle to minimize If a cow or heifer is bitten by a tick when 2 to 6 the impact of the disease. Farm advisors and specialists months pregnant, the calf may abort or be born weak. with knowledge of the tick’s feeding habitats and how Heifers and cows that have not previously grazed in the abortions developed in cattle used case studies tick-infested pastures are most susceptible. Once bit- with ranchers to develop management options that ten, cows appear to gain some degree of immunity, ranchers could use to lessen the impact of the disease but ranchers have observed that immunity can be lost if on their business. Successful practices included pre- cattle go for a year or more without tick bites, which serve as Pajaroello tick exposing sexually mature heifers to known tick areas prior an immunity booster. to breeding, avoiding tick areas during the critical 2 to 6 Early UC efforts focused on identifying the vector of the disease. months of pregnancy and shifting from spring to fall calving in the First, mosquitoes were suspected. They were eliminated as a pos- most northern regions of the state. sibility when cattle elevated off the ground (in an area where the SVM researchers and the California Animal Health and Food disease commonly occurred) carried their calves to term. Additional Safety (CAHFS) laboratory system, using a large number of aborted experiments also eliminated the Leptoconops gnat as a possible calves, were able to develop methods to identify foothill abortion in vector. aborted calves. This knowledge was extended to practicing veteri- It was initially thought that the Pajaroello tick did not live in the narians working with ranches throughout the state. most northern areas of California, where EBA occurred. When ticks In 2002, a SVM laboratory developed a reliable challenge system were subsequently trapped on a northern Lassen County ranch that for experimental transmission of EBA that was used to establish had experienced abortions, it was confirmed as a potential vector. that the causative agent was antibiotic susceptible. This report was Ticks were collected and placed to feed on susceptible heifers (on quickly followed with a positive identification of the agent causing the UC Davis campus), and abortions occurred, confirming the Paja- foothill abortion, a bacteria belonging to a very unusual group of roello as the vector of the disease. slime bacteria; then referred to simply as the agent of EBA, the bac- The next step was to determine the causative agent being terial pathogen has now been unofficially named Pajaroellobacter transmitted by the bite of the tick. This was difficult because the abortibovis. tick harbors numerous potential causative agents. In the late 1960s Tick photo: Will Suckow; specimen provided by Bohart Museum of Entomology

114 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 Other breakthroughs followed quickly. The cultivation of the on embryonic mortality in animals bred within weeks following vac- bacteria in immunodeficient mice gave new life to research efforts. cination. These studies are being conducted using a combination of A vaccine development phase was initiated with over $200,000 from UC and private producer replacement heifers. The vaccine dose is the California Cattlemen Association’s Livestock Memorial Research being adjusted downward, and the time from vaccination to breed- Fund and financial support from SVM and their collaborators at the ing is being extended. The vaccine cannot be administered to preg- University of Nevada, Reno. In 2009, a small group of heifers were nant cattle. Skin reactions following vaccination suggest that the live protected against experimental infection after they were immunized bacterial pathogen can persist for up to 2 months. On the positive several weeks prior to breeding with a candidate vaccine that was side, this bacterial persistence induces a solid immunity that likely both live and infectious. lasts through the next breeding cycle and possibly beyond. Studies The success of a second and larger trial in 2010 prompted SVM are under way to begin to address length of immunity. researchers to pursue product licensing with the U.S. Department of The fact that the vaccine is live and infectious poses several Agriculture (USDA) Center for Veterinary Biologics. Vaccine efficacy unique challenges. For example, the cryopreserved bacteria must experiments were conducted in accordance with USDA regulations. be transported and stored in liquid nitrogen, and the cost of pur- University-owned heifers were immunized before breeding and chasing the vaccine could also be high because of the cost of then administered an artificial challenge with virulent bacteria at the manufacturing — the live vaccine must be cultured in an immuno- peak of fetal susceptibility (100 days gestation). Vaccine field trials deficient mouse. The California Cattlemen’s Association is working that combined USDA-required field safety trials with field efficacy to develop a regional distribution system for the vaccine, which were then initiated at the UC Sierra Foothill Research and Extension could become available within a couple of years. Center on UC Davis Department of Animal Science heifers, on heifers Work is being conducted to develop a recombinant vaccine at University of Nevada, Reno, and on producer-owned beef herds in through genomic research. In a recombinant vaccine, the genomic California and Nevada. Over 1,600 heifers were enrolled in these tri- sequence of candidate bacterial genes must first be established. als in 2011 and 2012. Additional funding for such a massive effort was Next, the genes must be expressed as protein and then combined provided to the SVM by UC’s Office of the President via a UC Proof of with adjuvant(s) to construct candidate vaccines. A recombinant Concept Discovery Grant (grant ID no. 212263). vaccine would be far less sensitive to temperature and would not re- Although the results of these studies are currently being assem- quire immunodeficient mice in the manufacturing process, thereby bled, preliminary assessment of the experimental vaccine indicates making the finished product much more cost effective and practical excellent protection against foothill abortion has been successfully for on-ranch use. demonstrated. All the successes realized to date were a result of Subsequent findings by the SVM researchers have also improved SVM collaborations across the UC spectrum with CAHFS’s diagnostic the diagnostic procedures for identifying foothill abortions at the laboratory at UC Davis, the UC Davis Department of Animal Science, CAHFS diagnostic laboratory at UC Davis and have provided addi- UCCE, the Sierra Foothill Research and Extension Center, and also tional important information for UCCE to extend to ranchers to con- with researchers at the University of Nevada, Reno. firm abortions caused by the disease. Researchers are now actively Historically, specialty vaccines created for use only in California pursuing validation of a diagnostic assay that may allow ranchers in were licensed through the California Department of Food and Agri- the future to identify cows that have been exposed to the tick. Such culture (CDFA). Currently, CDFA does not process new specialty vac- an assay could be used to establish susceptibility of naïve replace- cines, requiring researchers to work with the USDA to get the foothill ment heifers to foothill abortion or confirm whether the disease is abortion vaccine licensed. USDA requirements are more stringent present on a ranch. than CDFA’s requirements, as food animal vaccines must comply Decades of hard work by UC researchers and educators all across with the federal Virus-Serum-Toxin Act requirements. SVM and USDA the system have allowed the pieces of this difficult disease puzzle to are charting new territory as they work to certify the safety and effi- come together in assisting California’s cattle ranchers. c cacy of the vaccine. The developers of the vaccine at SVM are in the process of establishing a USDA-required vaccine seed, determining if production can be scaled up to a commercial level and identifying viable options for commercial production of the vaccine. G.A. Nader is UC Cooperative Extension (UCCE) Livestock and Natural Resources As the commercialization efforts proceed, researchers are fine- Farm Advisor, Sutter, Yuba and Butte counties; M.N. Oliver is UCCE Staff Research Assistant, Retired; J.A. Finzel is UCCE Livestock and Natural Resources Advisor, tuning the vaccination regime to address concerns over the pro- Kern, Kings and Tulare counties; M.T. Blanchard is Specialist in longed persistence of the vaccine bacteria and the potential impact Pathology, Microbiology and Immunology, UC Davis School of Veterinary Medicine; and J.L. Stott is Professor of Pathology,

Microbiology and Immunology, UC Davis School of Zhukova Elëna References Veterinary Medicine. Blanchard MT, Chen CI, Anderson M, et al. 2010. Serial passage of the etiologic agent of epizootic bovine abortion in immunodeficient mice. Vet Microbiol 144(1–2):177–82. Bushnell R, Oliver M, Nader G, Norman B. 1991. Foothill Abortion. Veterinary Medi- cine Extension, Cooperative Extension, School of Veterinary Medicine, University of California, Davis. King DP, Chen C-I, Blanchard MT, et al. 2005. Molecular identification of a novel deltaproteobacterium as the etiologic agent of epizootic bovine abortion (foothill abortion). J Clin Microbiol 43(2):604–9. Stott JL, Blanchard MT, Anderson M, et al. 2002. Experimental transmission of epi- zootic bovine abortion (foothill abortion). Vet Microbiol 88(2):161–73.

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 115 Caltrans and others because of its drought Oleander 555 hardiness, it does have an impact on the animal population, which needs to be Nitrate accumulators 134 highlighted. The publication by Forero et Pyrrolizidine alkaloid 70 al. (2011) and the information provided also helped producers define the risk of Oxalate 49 plant poisonings. Avocado 22 The CAHFS laboratory system and UCCE also play an important role in Oak 28 poultry diseases. Many backyard poultry operations allow their birds to roam free Yew 14 and intermix with wild birds, and as a Yellow star thistle 13 result they represent a potential portal for the transmission of diseases such as avian Lupines 10 influenza from wild birds. Due to the rela- Foxtails 9 tive lack of veterinary clinics with poultry expertise, many backyard producers look 0 100 200 300 400 500 600 to UCCE livestock advisors to help them Diagnosis (no.) with routine management and disease Fig. 2. Livestock plant-poisoning cases, 1990–2007. identification during a disease outbreak. This partnership between Extension per- handling. In response to requests from by performing fundamental and applied sonnel and the CAHFS lab system is an the California Cattlemen’s Association, research on those same diseases and by important part of the effort to protect both the CAHFS lab system adopted a PCR- distributing the knowledge gained back commercial and noncommercial poultry based test that had originally been de- to producers. UC is also an important as well as the general public from dis- veloped by Dr. Bob BonDurant of SVM source for expert knowledge about live- eases originating in wild birds. (Ho et al. 1994). It has subsequently been stock diseases to both federal and state The CAHFS laboratory system and determined that the same degree of cer- regulatory officials on a regular basis and UCCE specialists have worked together to tainty that an animal is free of infection during disease outbreak emergencies. c define and test new diagnostic procedures can be provided by testing a single sam- that have higher accuracy or shorter turn- ple via PCR as was formerly gained by around times. For example, sampling of culturing three separate samples. This has bulls to test for trichomoniasis, a venereal resulted in a faster test turn-around time J.M. Adaska is Professor of Diagnostic Pathology, disease of cattle, requires that the animals and significantly less handling of bulls. California Animal Health and Food Safety Laboratory be gathered and restrained in a chute. UC continues to demonstrate its value System, School of Veterinary Medicine, UC Davis; E.R. Atwill is Professor, Department of Population Health When culture-based methods were in use, on a daily basis by playing an important and Reproduction, School of Veterinary Medicine, UC bulls had to be sampled three times to and wide-ranging role in the protection Davis; and G.A. Nader is UC Cooperative Extension be certain they were not infected, which of animal agriculture, by being heavily Livestock and Natural Resources Farm Advisor, Sutter, led to increased feed costs and potential involved in the surveillance for and diag- Yuba and Butte counties. trauma to the animals from repeated nosis of important diseases of livestock,

References Angelos JA. 2009. Infectious bovine keratoconjunctivitis. Atwill ER, Hou L, Karle BM, et al. 2002. Transport of Cryp- MacLachlan NJ, Mayo CE. 2013. Potential strategies for In: BP Smith. Large Animal Internal Medicine. St. Louis, Mis- tosporidium parvum oocysts through vegetated buffer control of bluetongue, a globally emerging, Culicoides- souri: Mosby Elsevier. p 1286–8. strips and estimated filtration efficiency. Appl Environ transmitted viral disease of ruminant livestock and wild- Angelos JA, Ball LM, Hess JF. 2007. Identification and Microb 68(11):5517–27. life. Antivir Res 99(2):79–90. characterization of complete RTX operons in Moraxella Atwill ER, Johnson E, Das Gracas M, Pereira C. 1999. Nolen RS. 2002. Exotic Newcastle disease strikes game bovoculi and Moraxella ovis. Vet Microbiol 125:73–9. Association of herd composition, stocking rate, and birds in California. J Am Vet Med Assoc 221(10):1369–70. Angelos JA, Gohary KG, Ball LM, et al. 2012. Randomized calving duration with fecal shedding of Cryptosporidium Pitesky M, Cataline K, Crossley B, et al. 2013. Historical, controlled field trial to assess efficacy of aMoraxella bovis parvum oocysts in beef herds. J Am Vet Med Assoc spatial, temporal, and time-space epidemiology of very pilin-cytotoxin-Moraxella bovoculi cytotoxin subunit 215(12):1833–8. virulent infectious bursal disease in California: A retro- vaccine to prevent naturally occurring infectious bovine Atwill ER, Partyka M, Bond RF, et al. 2012. An Introduction spective study 2008–2011. Avian Dis Mar 57(1):76–82. keratoconjunctivitis. Am J Vet Res 73:1670–5. to Waterborne Pathogens in Agricultural Watersheds. Rochelle PA, Jutras EM, Atwill ER, et al. 1999. Polymor- Angelos JA, Hess JF, George LW. 2001. Cloning and char- Nutrient Management Technical Note No. 9. Natural phisms in the beta-tubulin gene of Cryptosporidium par- acterization of a Moraxella bovis cytotoxin gene. Am J Vet Resources Conservation Service, US Department of Agri- vum differentiate between isolates based on animal host Res 62:1222–8. culture. p 1–84. but not geographic origin. J Parasitol 85(5):986–9. Angelos JA, Lane VM, Ball LM, et al. 2010. Recombinant Forero L, Nader G, Craigmill A, et al. 2011. Livestock- USDA NASS. 2012. US Department of Agriculture Na- Moraxella bovoculi cytotoxin-ISCOM matrix adjuvanted Poisoning Plants of California. UC ANR Pub 8398. Oak- tional Agricultural Statistics Service, Crop Year 2011. vaccine to prevent naturally occurring infectious bovine land, CA. http://anrcatalog.ucdavis.edu/pdf/8398.pdf. www.nass.usda.gov/Statistics_by_State/California/Publi- keratoconjunctivitis. Vet Res Commun 34:229–39. Ho MS, Conrad PA, Conrad PJ, et al. 1994. Detection of cations/California_Ag_Statistics/Reports/2011cas-all.pdf. Angelos JA, Spinks PQ, Ball LM, et al. 2007. Moraxella bo- bovine trichomoniasis with a specific DNA probe and Xiao L, Sulaiman IM, Morgan UM, et al. 2002. Host adapta- voculi sp. nov., isolated from calves with infectious bovine PCR amplification system. J Clin Microbiol 32(1):98–104. tion and host-parasite co-evolution in Cryptosporidium. keratoconjunctivitis. Int J Syst Evol Micr 57:789–95. Int J Parasitol 32:1773–85.

116 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 EXCLUDING PESTS AND PATHOGENS

Plant health: How diagnostic networks and interagency partnerships protect plant systems from pests and pathogens by Richard M. Bostock, Carla S. Thomas, Richard W. Hoenisch, Deborah A. Golino and Georgios Vidalakis

Early detection and rapid response are crucial in any effort to reduce the risk of new and the European grapevine moth. California emerging biological threats to crops and other plant resources. This underscores the is the leading U.S. state for agricultural products, with gross cash receipts in 2011 importance of having the necessary diagnostic expertise, infrastructure and resources in excess of $43 billion (CDFA 2013) for in place. Three programs — the National Plant Diagnostic Network, the National Clean more than 400 commodities, including Plant Network and the Citrus Clonal Protection Program — illustrate how accurate numerous specialty crops. In fact, seven and rapid diagnosis plays a critical role in providing healthy plants for growers and in of the top 10 commodities in terms of cash value in California are specialty crops. securing production systems for food and fiber. These three programs depend on state- All of this presents great opportunities, as wide, regional and national networking among university, state and federal scientists, well as risks and challenges, for diagnos- regulatory officials and industry members to help mitigate the impacts of plant pests tic, pest management and clean stock and and diseases. seed programs. During the past decade, awareness and concern have increased in regard to the lant pathogens and pests present introductions for which containment and threat of economic harm to U.S. crop ag- continual challenges to the produc- eradication have been unsuccessful, often riculture, nurseries and forests posed by Ption and security of food, fiber and with devastating consequences to agri- introduced biological agents, and society forest resources. Introduced biological culture and natural ecosystems (Pimentel has responded with greater investments agents threaten crops and forests locally et al. 2005; Rossman 2009). In California, in biosecurity programs to enhance sur- and regionally with their direct damage the past two decades have seen the emer- veillance and detection. Understandably, to host plants, and their presence has gence of a number of high-consequence exotic and high-consequence agents re- national and international consequences plant pests, including the sudden oak ceive the greatest focus in such programs, for trade and regulatory policy. Contami- death pathogen, the Pierce’s disease but it is important to note that sufficient nated seed and nursery plants provide pathogen (carried by the glassy-winged diagnostic infrastructure and expertise efficient introduction pathways for pests, sharpshooter) and more recently the must be continually maintained so we can highlighting the critical importance of Asian citrus psyllid, vector of the citrus accurately identify both routine and un- clean seed and nursery programs for greening disease (huanglongbing), and usual conditions. protection of both domestic and export markets. Introduced biological agents, whether they arrive via natural dispersal mechanisms or through human activ- M. E. Rogers ity, may remain present but below our threshold for detection and perception for years, only to emerge later with seeming suddenness and dramatic destructive in- tensity (Crooks 2005). As is the case in human and animal medicine, early detection, accurate di- agnosis and rapid response are critical for achievement of successful outcomes when dealing with outbreaks of endemic and newly introduced plant diseases and insect or weed pests. The United States has a long history of pathogen and pest

Online: http://californiaagriculture.ucanr.edu/ landingpage.cfm?article=ca.v068n04p117&fulltext=yes doi: 10.3733/ca.v068n04p117 Heavy infestation of Asian citrus psyllids (Diaphorina citri) on Murraya. Inset, adult psyllid.

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 117 Even with recent investments in plant of information and expertise about new delivers advanced training for diagnosti- biosecurity programs, the immensity detections in order to minimize their eco- cians and educational programs for “first of the task exceeds the resources cur- nomic and ecological impacts (Stack et al. detectors,” facilitates communication rently available to adequately address it. 2006; Stack et al. 2014). among plant diagnosticians at LGUs, state For example, the most significant path- Federal funding for the establishment departments of agriculture and national way for introduction of unwanted plant of the NPDN and a parallel program for expert laboratories, and seeks to provide pathogens and pests is through live plant animal agriculture, the National Animal accurate and timely information to state imports, which have increased, on aver- Health Laboratory Network (NAHLN), and federal authorities to guide an ap- age, by 51 million plants per year for the was largely a response to biosecurity propriate response. For greater efficiency past 43 years (Liebhold et al. 2012; Palm risks to plant and animal agriculture in in program delivery, the NPDN is divided and Rossman 2003). In 2010, more than the United States. Also compelling for into five geographic regions, each with a 2.8 billion plants intended for planting decision-makers at the time was a grow- regional center located in the plant pathol- within the United States passed through ing awareness that many publicly funded ogy department of an LGU (fig. 1), where federal plant inspection stations at U.S. plant diagnostic labs associated with its directors help identify and coordinate ports of entry. This sheer volume of plants land-grant universities (LGUs) and state local and regional scientific expertise in by itself reduces the likelihood that all of departments of agriculture were in fact plant pathology, entomology and weed/ the potentially invasive pests and patho- underfunded and were, in some cases, plant science as needed. The NPDN does gens will be intercepted, and that in turn at risk of closure as a result. In addition, not have any formal regulatory authority makes downstream programs for detec- it appeared that a lack of coordination of its own; rather, the network’s principal tion, diagnosis and containment all the among diagnosticians and experts at role is to provide a framework that facili- more important. university, state and federal laboratories tates access to additional expertise in the could create bottlenecks in the processing event of a plant health emergency. The National Plant Diagnostic Network of critical samples and delays in commu- Given the agricultural diversity of The National Plant Diagnostic nication of diagnostic results. the United States, the regionally dis- Network (NPDN) was established in 2002 The NPDN is supported in part tributed structure of the NPDN enables to provide greater support for and inte- by the USDA’s Food and Agriculture each region to tailor the resources and gration of plant diagnostic laboratories Defense Initiative (FADI), a program programs it provides to best meet the in the United States and help thwart the within the National Institute of Food needs of that particular region. For ex- establishment and dispersal of introduced and Agriculture (NIFA). To further its ample, the Western region includes 10 insect and weed pests and pathogens core missions of diagnostics, training Western states and U.S. Pacific territories (npdn.org/). The NPDN works with and education, and communication, the that partner to form the Western Plant state and federal agencies to ensure the NPDN provides resources for diagnostic Diagnostic Network (WPDN; wpdn.org/). quick, accurate and secure conveyance laboratory infrastructure and supplies, The regional center, located at UC Davis,

Great Plains Diagnostic North Central Plant Northeast Plant WPDN Regional Center, Network, Kansas State Diagnostic Network, Diagnostic Network, UC Davis/CDFA University Michigan State Cornell University University

Alaska

NPDN National Repository, CERIS, Purdue University American Samoa Hawaii

Guam Expert/sentinel labs Southern Plant Diagnostic Network, Triage labs Puerto Rico University of Florida

Fig. 1. Organizational map of the National Plant Diagnostic Network with the five regional networks and the NPDN National Repository at Purdue University. The Western Plant Diagnostic Network (WPDN) includes 10 Western states and U.S. territories in the Pacific.

118 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 works in partnership with the California discern patterns of new outbreaks at vari- diagnostics are often sent directly to UC Department of Food and Agriculture ous scales of resolution and in relation laboratories that have the appropriate (CDFA) Plant Pest Diagnostic Center, to GIS-based platforms for weather and expertise. If the pest or pathogen is sus- which is the formal diagnostic report- land use. pected to be new to California or to the ing authority for California (cdfa.ca.gov/ Path of a suspect sample. An impor- county where it was found, a confirma- plant/PPD/). tant contribution of the NPDN has been tory diagnosis must be made by CDFA The scope and size of agricultural, the education of first detectors in the scientists, and may require further sam- nursery and forest production systems, proper procedure to follow when sub- pling. When a pest or pathogen is sus- as well as infrastructure and expertise in mitting samples to diagnostic labs (fig. pected to be new to the United States or support of plant health programs, vary 2). In California, a first detector may be to North America, samples are sent to the considerably throughout the WPDN, with a grower, crop consultant, pest control USDA Animal Plant Health Inspection three subregional expert laboratories that adviser, UC researcher, UC Cooperative Service (APHIS) National Identification work together with the various triage Extension (UCCE) farm advisor, biolo- Services, where specialists at federal, state laboratories in individual states and ter- gist within a county agriculture com- or university laboratories with expert ritories. The three expert laboratories — missioner’s office, UC-trained master knowledge about the suspect agent are the CDFA laboratory in Sacramento and gardener, employee of a city or county consulted for a confirmatory diagnosis. diagnostic laboratories at Oregon State parks department or homeowner — re- How the NPDN has made a difference. University (Corvallis) and the University ally, any person who has been trained to Perhaps the most important contribu- of Hawaii (Manoa), working in partner- recognize potential threats to plant health tion of the NPDN has been to foster an ship with the Hawaii Department of and understands the importance of plant unprecedented level of coordination Agriculture — can handle most or all biosecurity, and who knows how types of samples and conduct collabora- to collect and submit a sample tive diagnostics with other member labo- securely. ratories in the region or the nation. The Typically, the first detector re- CDFA laboratory is the largest and most trieves a suspect sample from the comprehensive state plant diagnostic field, packages it properly and de- Field sample from rst detector laboratory in the United States, with more livers or mails it to the county ag- than 70 scientists and support staff spe- ricultural commissioner or cializing in pests, diseases, weeds, nema- UCCE county office. There, todes and seed certification. It receives it is identified or sent to County expertise: Agricultural commissioner’s little funding from the NPDN, relative to the CDFA laboratory in oce or Extension agent/farm advisor the scope and size of the laboratory’s ac- Sacramento for further tivities, drawing its primary support from analysis and diagnosis by state funds and other grants. a specialist. Some samples If unknown or nonregulated Similar to the WPDN, the other four that require specialized regional networks in the NPDN are con- sortia of LGUs and state departments of Triage NPDN diagnostic lab (university or agriculture working together to support local state dept. of agriculture) mission-related activities and provide diagnostic services. Diagnostic results from NPDN member laboratories in If unknown all 50 states and three U.S. territories are submitted to the NPDN National Repository at Purdue University’s Center Identi ed for Environmental and Regulatory Regional NPDN diagnostic lab sample record Information Systems (CERIS; ceris. purdue.edu/npdn/). At the time of this writing (September 2014), the repository If unknown or if federally regulated houses more than 930,000 diagnostic and requires con rmation sample records in a database that is up- dated daily; it receives about 100,000 new NPDN National records each year from as many as 150 Repository USDA APHIS National Identi cation Services laboratories throughout the nation. Such a comprehensive national database of diag- nostic records is unprecedented in plant agriculture. It is available for search and State or federal regulatory response if necessary (e.g., containment and eradication) analysis by authorized scientists, regula- tory officials and diagnosticians who use Fig. 2. Path of a field sample from first detector through the diagnostic process and ultimately to being it to rapidly identify novel detections and archived as a record in the NPDN National Repository.

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 119 and communication among the nation’s than 2,500 registered first detectors, of introduction of exotic pests that, once diagnostic laboratories. For example, in the WPDN training coordinator and introduced, can be difficult and costly the event of a regional or national plant UCCE specialists and farm advisors and to control. health emergency, instead of overwhelm- other UC Division of Agriculture and The original impetus for the organiza- ing one laboratory with samples, the Natural Resources (ANR) personnel tion of networks with a focus on clean distributed network structure provides work together to conduct trainings and stock came from the U.S. grape and fruit a more flexible surge capacity, eliminat- workshops. These are offered in con- tree industries, which in 2005 began to ing bottlenecks that could hamper the junction with experts at universities, the explore the formation of a national group diagnostic and reporting process (see CDFA and the USDA APHIS and USDA devoted to foundation materials that have sidebar, page 121). In addition, through Agricultural Research Service (ARS) to been tested, treated and maintained as its regional networks and in partnership ensure network-wide consistency and a healthy source of plant materials for with USDA APHIS, the NPDN has made preparedness of diagnostic labs. growers to use. In 2008, these grape and significant investments in laboratory fruit tree networks were developed by The National Clean Plant Network infrastructure, equipment, supplies and stakeholders, industry members, scien- distance diagnosis capabilities, and it Healthy planting stock is key to the tists and other interested parties. The new has provided partial salary support and cost-effective production of horticultural National Clean Plant Network (NCPN) advanced training for scientific and tech- crops such as fruit trees, nut trees and was included in the 2008 and 2014 Farm nical staff. grapevines. Healthy stock is easier to Bills, with funding of $5 million per year Another important accomplishment propagate, requires fewer chemical inputs to provide reliable sources of propagative of the NPDN is the development and and produces higher crop yields and material that are free of graft-transmitted delivery of training and education pro- better crop quality. The U.S. agricultural pathogens. Congress stipulated that fund- grams for first detectors and diagnosti- sector needs healthy planting stock to ing go exclusively to existing clean plant cians. The NPDN’s national registry now keep it internationally competitive and centers that were already supported by includes more than 16,000 first detectors economically viable. The most efficient their home institutions. who can be alerted quickly to new out- approach to producing healthy planting The NCPN is a voluntary associa- breaks and who receive regular updates stock is through programs that screen tion made up of specialty crop networks via national and regional e-newsletters valuable plant selections for viruses and that promote the use of pathogen-tested, with useful information about new pests other diseases that have the potential to healthy plant material for U.S. growers and pathogens of regulatory concern. be spread through contaminated plant of grapes, fruit trees, hops, berries and In California, currently boasting more stock. Quarantine services provided by citrus. Its formal mission is to “provide clean stock programs reduce the chances high quality asexually propagated plant material free of targeted plant pathogens and pests that cause economic loss to 19 18 11 3 1. Auburn University, Auburn, Alabama 2. Clemson University, South Carolina 8 3. Cornell University, Geneva, New York 15 4. Florida Department of Agriculture and Consumer Service, Gainesville 9 5. Florida Department of Agriculture and 16 10 Consumer Service, Winter Haven 14 2 6. Florida A&M University, Tallahassee 13 7. Louisiana State University, Baton Rouge 1 8. Michigan State University, East Lansing 9. Missouri State University, Mountain Grove 7 6 4 10. North Carolina State University, Raleigh 12 5 11. Oregon State University, Corvallis 12. Texas A&M University (TAMUK), Kingsville 13. University of Arizona, Yuma 14. University of Arkansas, Fayetteville 15. University of California, Davis 17 16. University of California Riverside, in collaboration with USDA ARS National Clonal Hawaii Germplasm Repository for Citrus and Dates 17. University of Hawaii, Honolulu Alaska 18. USDA ARS, Corvallis, Oregon 19. Washington State University-IAREC, Prosser

Fig. 3. The 19 regional centers of the National Clean Plant Network (NCPN).

120 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 protect the environment and ensure the global competitiveness of specialty crop producers.” By agreement, it operates un- A broad lab network means greater der the auspices of three federal agencies flexibility and better response — USDA APHIS, ARS and NIFA — which cooperatively support its research, quar- he “surge capacity” of the National Plant Diagnostic Network (NPDN) was instru- antine and outreach activities. Tmental in providing support for several investigations of Phytophthora ramorum, the USDA funding supports existing clean cause of sudden oak death in coastal forests and ramorum blight of ornamentals (Rizzo plant centers that have the expertise, et al. 2005). In 2004, P. ramorum was unexpectedly detected in several Southern Califor- facilities and appropriate climates to ef- nia production and wholesale nurseries that had already shipped 2.3 million potentially ficiently produce, maintain and distribute infected plants to retail nurseries and other wholesale nurseries in 49 states and the healthy planting stock for those crops. District of Columbia. This triggered a national regulatory response to determine where Advisory committees that include indus- plants had been shipped and then, once found, to test the plants for P. ramorum. try representatives and researchers from Over the next year, federal and NPDN labs processed more than 100,000 samples. throughout the country make up an es- Because of the NPDN laboratories’ advanced coordination and training, they were able sential part of the equation for communi- to rapidly implement the standardized APHIS diagnostic protocol with little advance cating priorities to the NCPN. notice. One critical element of this protocol is a molecular diagnostic based on the PCR NCPN centers. As of this writing, assay, which at the time was newly developed by APHIS and UC scientists. In addition, the NCPN network includes 19 clean the NPDN provided support for the purchase of PCR machines and supplies and re- plant centers (fig. 3). Each of the five cur- agents that enabled many network labs to participate. In total, 171 nurseries in 20 states rent crop programs has one program tested positive for P. ramorum, triggering implementation of containment and eradica- that serves as its administrative lead. tion measures at those sites. A national website (nationalcleanplant Prior to establishment of the network, it could take 6 weeks or more for samples to network.org) maintained by the staff of go through the system, and nursery plants were quarantined until diagnosis could be Foundation Plant Services (FPS) at UC completed. With the NPDN labs and the new diagnostic assay, turnaround times from Davis has links to a website for each of field collection to diagnosis were reduced to as few as 4 days, enabling many nurseries the NCPN crops maintained by the ad- around the country to quickly resume operations once they had been cleared as free ministrative lead center. UC Davis is ad- from P. ramorum. c ministrative home for the grape network. The NCPN berries group — the Berry Crops Testing, Therapy and Diagnostics Development Program — is headquar- tered at the USDA Horticultural Crops Research Unit, USDA ARS, in Corvallis, Parke Jennifer Oregon. The citrus network home is with the Citrus Clonal Protection Program (CCPP) at UC Riverside (see below). Both the fruit tree network and the hops net- work are housed at Clean Plant Center Northwest, Washington State University‐ IAREC, in Prosser, Washington. Citrus Clonal Protection Program The CCPP has its roots in the 1930s, when Professor Howard Fawcett of the UC Citrus Experiment Station in Riverside discovered the viral nature of the graft-transmissible disease citrus psorosis — the discovery that triggered the establishment of the Psorosis Free Program. Following a request from the citrus industry, UC established what is now the CCPP in 1956, initially calling it the Citrus Variety Improvement Program. Today the CCPP stands as a cooperative program of UC Riverside’s Department of Roubtsova Tatiana Plant Pathology and Microbiology, CDFA, Rhododendron plants declining from ramorum blight caused by Phytophthora ramorum in a USDA APHIS and the NCPN, as well as commercial nursery. Inset, leaf symptoms of ramorum blight on Rhododendron. the state’s citrus industry as represented

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 121 by the California Citrus Nursery Board Riverside campus and the Foundation Marketing Orders), while UC Riverside (CCNB) and the Citrus Research Board and Evaluation Blocks at the UC Lindcove offers infrastructure support and scien- (CRB). Research and Extension Center, in Exeter, tific expertise. A committee of industry The CCPP operates at three loca- California. The CCPP is supported by the members (growers and nursery people) tions: the Rubidoux Quarantine Facility CRB and CCNB (industry organizations supports the CCPP activities. in downtown Riverside, the Citrus founded in 1968 and 2005, respectively, in The CCPP is the basic element of a Diagnostic Laboratory on the UC response to the California State Handler long-term, multilevel program whose

Budwood introduction and primary increase

Foreign origin Domestic origin California origin (not California)

Therapy Thermotherapy and/or Initial index shoot-tip grafting Biological and/or laboratory

Time at the quarantine Tested positive Tested negative CCPP facility Rubidoux approximately Quarantine 24-36 months. Facility Varies, depending Variety index (VI) and Citrus on the pathogen Diagnostic Biological and laboratory. load of the All known graft-transmissible pathogens Laboratory, introduction. UC Riverside

Tested negative*

Release from state and federal quarantine

Proprietary varieties delivered to owners

Propagation of budwood source trees

CCPP Protected foundation blocks. Budwood Foundation and evaluation eld Foundation source trees routine retesting for blocks. Budwood source trees and and graft-transmissible pathogens trueness-to-type evaluation Evaluation Blocks, Lindcove Research and Extension Budwood distribution. Worldwide with priority of Center, California demand for use by the commercial Exeter industry, research, and variety improvement

Fig. 4. Flow chart for citrus budwood introduction, propagation of source trees and distribution conducted by the Citrus Clonal Protection Program (CCPP). * To fulfill movement requirements between quarantine zones, all materials must undergo therapy regardless of the pre-index results.

122 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 objectives include avoiding or restricting and longevity. In addition, diseases from and also demonstrate that environmental the spread of bud- and graft-transmitted infected field propagation may spread to conditions in the greenhouse are optimal pathogens of citrus in support of a profit- neighboring orchards via insects or con- for plant growth and symptom expression able, competitive and sustainable citrus taminated farm equipment (Timmer et al. (Childs 1978; Roistacher 1991; Vidalakis et industry. As such, the CCPP provides a 2000; Wallace 1978). al. 2004). safe mechanism for the introduction of Disease diagnosis and pathogen detec- Citrus propagative material (i.e., bud- citrus varieties into California from any tion take place in the insect-proof green- wood) distributed to homeowners, hobby- area around the world. The process for house and the Delfino Plant Laboratory at ists, citrus growers and nurseries draws varietal introduction includes disease the Rubidoux Quarantine Facility as well from tree sources of the CCPP foundation diagnosis and pathogen elimination fol- as in the Citrus Diagnostic Laboratory at block. All CCPP- and nursery-owned lowed by maintenance, pathogen retest- UC Riverside. Detection of graft-transmis- citrus budwood tree sources must be ing and distribution of true-to-type citrus sible citrus diseases is based on a com- established and propagated from citrus propagative material (fig. 4). prehensive indexing scheme that involves material that has been through the CCPP The CCPP program of importation, biological and laboratory diagnostics. introductory, therapy and diagnostic pro- production and distribution of pathogen- For biological indexing, technicians graft tocols, regularly and routinely tested for tested propagative materials is based tissue from the imported budline onto several citrus pathogens, and registered on a comprehensive indexing (testing) citrus indicator plants, with a specific as a budwood source with the CDFA. In program to detect graft-transmissible citrus indicator for each specific disease. May 2010, CDFA filed regulations for a diseases and pathogens that may arrive Indicator varieties have been selected for mandatory Citrus Nursery Stock Pest in imported budlines. Graft-transmissible their sensitivity to diseases and their abil- Cleanliness Program as an emergency ac- diseases may be caused by viruses, vi- ity to express symptoms. For each index, tion. Under this new mandatory program, roids or other pathogens (e.g., bacteria, technicians maintain adequate positive more than 8,000 registered budwood phytoplasmas) and are vegetatively trans- control plants under the same environ- source trees were tested for several citrus mitted with an infected budline. Graft- mental conditions as the test indicators. pathogens in the first 2 years. The CCPP transmissible diseases can seriously harm The controls serve dual purposes: They and UC Riverside researchers have been fruit quality, production and tree health provide a comparison for the test plant instrumental in the development of a

A B Elizabeth Grafton-Cardwell Elizabeth

C David J. Gumpf J. David Therese Kapaun Therese

D E

Fig. 5. Panoramic view of the Citrus Clonal Protection Program Protected Foundation Block in the UC Lindcove Research and Extension Center in Tulare County. (A) The first screenhouse (40,000 sq ft) was constructed between 1998 and 1999, (B) the second screenhouse (30,000 sq ft) was completed in 2010 and (C) the positive pressure greenhouse (5,700 sq ft) was completed in 2011. The interior of the screenhouses with both (D) container and (E) in-ground budwood source trees.

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 123 high-throughput nucleic acid extraction research to move forward. The only way the speed with which samples can be and purification procedure optimized we can meet these goals is through a processed and put our general prepared- for citrus budwood tissues as well as program like the CCPP that works col- ness to address plant health emergencies molecular diagnostic methods for detec- laboratively with state and federal regula- at risk. Increases in agricultural trade tion of citrus pathogens. These efforts tors, the citrus industry and UC to release and plant importation, together with the have enabled the successful implemen- pathogen-tested citrus varieties. importance of sustainable production sys- tation of the new § 3701 CDFA Citrus tems for food and fiber, mean that the de- Partnerships for plant health Nursery Stock Pest Cleanliness Program mand for integrated programs to provide (Vidalakis and Wang 2013; CDFA permits The three programs described here accurate, rapid diagnoses in support of QC 1354 and QC 1388, www.cdfa.ca.gov/ demonstrate how investments in diagnos- plant health has never been greater. c plant/pe/nsc/nursery/citrus.html). tics, germplasm screening and develop- Since 2009, CCPP has supplied 154,000 ment, and related training and education buds from 301 different citrus varieties. are helping to safeguard agriculture and A citrus nursery can produce as many as plant resources at statewide, regional and R.M. Bostock is Plant Pathologist, California Agricultural Experiment Station, and Professor and Director, Western 300 trees within a year to 18 months from national levels. These programs provide Regional Center of the NPDN, Department of Plant each CCPP bud. That means that an esti- the agricultural industry with healthy Pathology, UC Davis; C. Thomas is Associate Director, mated 231 million citrus trees have been planting stock as well as highly coor- Western Regional Center of the NPDN, Department of produced from pathogen-tested CCPP dinated systems to deal efficiently with Plant Pathology, UC Davis; R.W. Hoenisch is Training and material in the past 5 years alone. If a sin- disease and pest outbreaks. Their success Education Coordinator, Western Regional Center of the gle pathogen had been present in any of is due to the commitment of resources by NPDN, Department of Plant Pathology, UC Davis; D.A. the buds used for this tree propagation, it the USDA, state agencies, industry and Golino is Director, Foundation Plant Services, and UC Cooperative Extension Specialist, Department of Plant would have been transmitted to millions LGUs. Pathology, UC Davis; and G. Vidalakis is Director, Citrus of trees, with unknown horticultural, pro- Especially critical to the success of Clonal Protection Program, Assistant Plant Pathologist, duction and economic effects. these programs in California are the con- and Assistant UC Cooperative Extension Specialist, Diseases can sometimes become so tributions of ANR and CDFA scientists Department of Plant Pathology, UC Riverside. important in citrus production that it may and support staff. Yet recent limitations in be necessary, for example, to change from state and federal funding for agricultural a long-used rootstock to one that is more science have put the continuation of these tolerant or resistant to a disease agent. programs in serious jeopardy. Reduced Such was the case when citrus tristeza funding will weaken interagency col- disease became a limiting factor for citrus laboration and sharing of expertise, limit production in California. Millions of trees training and education programs, reduce growing on sour orange rootstock, which was susceptible to tristeza quick decline, had to be replaced with trees grown on References tristeza-tolerant rootstocks of trifoliate Barnier JB, Grafton-Cardwell E, Polek M. 2010. Citrus Rizzo DM, Garbelotto M, Hansen EA. 2005. Phytophthora tristeza virus (CTV): Then and now. Citrograph 6:16–23. ramorum: Integrative research and management of an and trifoliate hybrids. The availability Calavan CE, Mather SM, McEachern EH. 1978. Regis- emerging pathogen in California and Oregon forests. of pathogen-tested tristeza-tolerant root- tration, certification, and indexing of citrus trees. In: Annu Rev Phytopathol 43:309–35. stocks and scions (e.g., mandarins) from Reuther W, Calavan EC, Carman GE (eds.). The Citrus In- Roistacher CN. 1991. Graft-transmissible diseases of cit- dustry (Vol. IV): Crop Protection. Berkeley, CA: University of rus. Handbook for detection and diagnosis. Rome: Food the CCPP was critical to the industry’s California, Division of Agricultural Sciences. p 185–222. and Agriculture Organization of the United Nations transition and subsequent economic suc- [CDFA] California Department of Food and Agriculture. (FAO). www.fao.org/docrep/t0601e/t0601e00.HTM. cess (Barnier et al. 2010; Calavan et al. 2013. California Agricultural Statistics Review 2012– Rossman A. 2009. The impact of invasive fungi on agri- 2013. California Department of Food and Agriculture, cultural ecosystems in the United States. Biol Invasions 1978). The availability of a wide selection Sacramento, CA. 131 p. 11(1):97–107. of citrus species, varieties and selections Childs JFL (ed.). 1978. Indexing Procedures for 15 Virus Stack JP, Bostock RM, Hammerschmidt R, et al. 2014. The for evaluation and experimental use is Diseases of Citrus Trees. Agricultural Research Service– National Plant Diagnostic Network: Partnering to pro- essential to our ability to address new United States Department of Agriculture, Washington, tect plant systems. Plant Dis 98:708–15. DC. Stack J, Cardwell K, Hammerschmidt R, et al. 2006. and emerging problems such as citrus Crooks JA. 2005. Lag times and exotic species: The ecol- The National Plant Diagnostic Network. Plant Dis greening. ogy and management of biological invasions in slow- 90(2):128–136. Another important factor for the health motion. Ecoscience 12(3):316–29. Timmer LW, Garnsey SM, Graham JH. 2000. Graft-trans- Liebhold AM, Brockerhoff EG, Garrett LJ, et al. 2012. missible, systemic diseases. In: Compendium of Citrus and sustainability of the commercial Live plant imports: The major pathway for forest insect Diseases. St. Paul, Minnesota: APS Press. p 51–69. citrus industry is maintenance of our and pathogen invasions of the US. Front Ecol Environ Vidalakis G, Garnsey SM, Bash JA, et al. 2004. Efficacy of capacity to import new varieties having 10(3):135–43. bioindexing for graft-transmissible citrus pathogens in different or improved fruit qualities or Palm ME, Rossman AY. 2003. Invasion pathways of ter- mixed infections. Plant Dis 88(12):1328–34. restrial plant-inhabiting fungi. In: Ruiz JM, Carleton JT Vidalakis G, Wang J. 2013. Molecular method for different maturity dates and organoleptic (eds.). Invasive Species: Vectors and Management Strate- universal detection of citrus viroids. US Patent No. characters to satisfy ever-changing con- gies. Washington, DC: Island Press. p 31–43. 20,130,115,591. sumer demands. A capacity to import and Pimentel D, Zuniga R, Morrison D. 2005. Update on the Wallace JM. 1978. Virus and viruslike diseases. In Reuther environmental and economic costs associated with maintain new pathogen-free citrus germ- W, Calavan EC, Carman GE (eds.). The Citrus Industry (Vol. alien-invasive species in the United States. Ecol Econ IV): Crop Protection. Berkeley, CA: University of California, plasm is imperative to keeping risk to 52(3):273–88. Division of Agricultural Sciences. p 69–72. the industry at a minimum and enabling

124 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 MANAGING NEWLY ESTABLISHED PESTS AND DISEASES hen new pests or diseases become established, they often lack the natural control of their native Wenvironments and develop into more serious problems when interacting with local plant or animal systems or local management practices. The response to constrain and manage them must be complex and coordinated between research institutions and scientists, government agencies and the agricultural community. The articles in this section profile two successful multi-partner responses to newly established threats to one of California’s premier commodities.

Growers, scientists and regulators collaborate on European grapevine moth program by Monica Cooper, Lucia Varela, Rhonda Smith, David Whitmer, Gregory Simmons, Andrea Lucchi, Roxanne Broadway and Robert Steinhauer

The first detection of the European grapevine moth in North America triggered the scientists and grape growers aimed to establishment of federal and state regulatory programs that (1) identified the insect’s control, contain and potentially eradicate insect populations. The cooperative effort geographic range in California, (2) developed and implemented detection and man- to develop and implement this program is agement programs, (3) regulated the movement of plant material and equipment to the focus of this article. minimize the threat of dispersal, (4) incorporated research-based information devel- Seasonal biology in California vineyards oped by subject-matter experts into policy decisions and (5) promoted a wide-reaching The European grapevine moth educational program for grape growers, the public and local officials. The action plan, (EGVM) may complete two to five annual developed and carried out through a coordinated program that included multiple generations, as determined by latitude, government agencies, university scientists and the agricultural community, drastically climate and microclimate (Ioriatti et al. reduced insect populations and limited the distribution in California vineyards such that 2011); temperature models predict three generations per year in the Napa Valley, some previously infested areas were removed from quarantine regulation. which has been validated through ground observations (Gutierrez et al. 2012). Pupae overwinter in diapause (a rest- nvasive species increasingly threaten the first detections were in Napa County, ing state) inside silken cocoons in pro- agricultural sustainability in a global California, where this invasive pest and tected locations, such as under the bark Ieconomy. If an invasive species is a associated fungal rot caused significant of the vine. The first male flight gener- known pest or assessed as potentially crop damage in 2009. A coordinated ally begins slightly before budbreak and threatening, its detection in California program by USDA, CDFA, county agri- may continue for 10 to 14 weeks. Adults may trigger a regulatory response coordi- cultural commissioners, UC, international generally fly at dusk when temperatures nated by the U.S. Department of Agricul- ture (USDA), the California Department of Food and Agriculture (CDFA) and agricultural commissioners. Regulatory Jack Kelly Clark Jack Kelly programs often encompass activities such as trapping, quarantine and treatment protocols, and depend on reliable scien- tific information generated by university researchers. European grapevine moth, Lobesia botrana (Denis & Schiffermüller), is endemic to Mediterranean Europe, has invaded portions of the Palearctic region (Europe, west Asia and North Africa) and East Africa, and was detected for the first time in the Americas in Chile, April 2008; in California, September 2009; and in Argentina, April 2010 (Ioriatti et al. 2012; Varela et al. 2013a). In the United States,

Online: http://californiaagriculture.ucanr.edu/ landingpage.cfm?article=ca.v068n04p125&fulltext=yes In 2009, European grapevine moth was first detected in the United States in Napa County, where it doi: 10.3733/ca.v068n04p125 caused significant crop damage.

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 125 are above 53.5°F (12°C). During the first flight, the female glues single eggs to flat surfaces on or near the flower cluster; second-

Monica Cooper and third-generation eggs are laid on grape berries. Larvae form webbed nests; the first-generation larvae feed on flowers before and during bloom in Northern California; second-generation larvae feed on green berries; and third-generation larvae feed inside ripening berries. Larvae create distinctive round holes in prebloom flowers and ripening fruit, which distinguishes their feeding damage from that of other common Lepidoptera larvae found in California vineyards (photo, left). Feeding damage to berries by second- and third-generation larvae exposes them to infection by Botrytis and other secondary fungi (photo, below Feeding damage by European grapevine moth larva to a grape flower left) that can be economically damaging. before bloom. Note the characteristic hole in the flower, webbing and larval excrement. Quarantine programs On October 7, 2009, USDA confirmed the presence of EGVM in Napa County. A federal order issued by USDA in June 2010 initiated a quarantine area within 5 miles (8 kilometers [km]) of Andrea Lucchi Andrea all detections (USDA 2010). Detections were defined as two or more adult moths trapped within 3 miles (5 km) of each other during the same life cycle or immature stages confirmed to be EGVM by DNA analysis. The order indicated plant host species as well as plant parts, products, farming and processing equip- ment, and green waste residues as regulated articles that could not be transported interstate from a quarantine area except under specific conditions. The state interior quarantine (CDFA 2012) enforced restrictions parallel to those in the federal order for intrastate movement of regulated articles within or from quarantine areas. In 2012, the quarantine buffer was reduced from 5 miles to 3 miles (5 km) around detections. This change accommodated the program’s need to reduce the cost of imple- mentation while acknowledging the adult moths’ short-distance natural dispersal (Boller 1993; Schmitz et al. 1996). Statewide survey and detection program Immediately after the first confirmed detection in 2009, USDA, CDFA and the Napa County agricultural commissioner deployed 248 sex pheromone–baited traps to delimit the popula- tion. However, very few moths were caught because traps were Feeding damage to grape berries by second- and third-generation larvae deployed at the end of the third flight (table 1). In addition to the exposes them to fungal infections that can be economically damaging. trap captures, ground surveys in 2009 recorded 26 larvae, eight

TABLE 1. European grapevine moths captured in pheromone-baited traps, presented by California county and by year (2009–2014)

Year Napa Sonoma Solano Mendocino Fresno Merced San Joaquin Santa Cruz Santa Clara Monterey Nevada ...... Number of male moths (number of traps) ...... 2009 5 (248) 2010 100,831 59 11 36 11 4 2 1 3 1 0 (3,882) (6,932) (1,514) (1,594) (8,648) (860) (3,522) (449) (596) (1,733) (55) 2011 113 9 0 0 0 0 0 1 19 0 4 (4,930) (9,048) (2,644) (2,237) (11,013) (1,502) (7,537) (552) (1,346) (2,651) (1,902) 2012 77 0 0 0 0 0 0 0 0 0 0 (4,706) (8,393) (1,844) (1,432) (8,630) (86) (4,714) (318) (658) (2,033) (920) 2013 40 0 0 0 0 0 0 0 0 0 0 (11,621) (6,906) (1,383) (1,430) (7,651) (1,265) (1,301) (202) (267) (1,998) (60) 2014* 0 1 0 0 0 0 0 0 0 0 0 (11,574) (7,011) (ND) (1,468) (2,169) (828) (4,243) (ND) (ND) (1,978) (ND) * These are preliminary values, as of July 30, 2014; final values will be available in November 2014; ND = no preliminary data available.

126 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 C h il es P pupae and one female at multiple sites in o pe Va l le two distinct areas of Napa County. As a y result, the state interior quarantine was Rd established in March 2010, over an area K n o

xv totaling 162 square miles (420 square kilo- il le

R meters [km2]) in Napa County (fig. 1). d In February 2010, trapping efforts St. 128 expanded throughout all grape-growing Helena regions of California — roughly 803,000 acres (325,000 hectares [ha]). Traps were deployed at densities of nine to 16 or 25 NAPA traps per square mile of planted vineyard COUNTY (three to six or 10 traps per km2) outside and inside the regulated area, respec- tively (table 1). In select urban areas, traps 121 were placed on potential EGVM host Yountville plants at a density of five traps per square SONOMA mile (two traps per km2) (Mastro et al. COUNTY 29 2010). By the end of 2010, the quarantine W o 12 o area included portions of eight California d e n V a l counties, totaled 2,091 square miles le y R (5,416 km2) and contained approximately d

L in 150,760 acres (61,010 ha) of vineyards (fig. d A a r n V o is l 2, table 2). Subsequently, in 2011, traps de- d t a

D A r v Ave e ln tected moths in two additional counties, Linco 1 st SOLANO bringing the total number of regulated Sonoma St Napa t W d S t 3 r COUNTY counties to 10 and a peak quarantine area S

h t 2 5 of 2,335 square miles (6,048 km ) (fig. 2, N apa R table 2). Trap captures in Napa County d indicated a large, widely distributed

221 G

r population, whereas populations in other 116 e e n counties were significantly smaller and V a l le y more contained (table 1). R d The EGVM regulatory program has relied heavily on the use of pheromone- EGVM state interior quarantine baited sticky traps to detect moth popula- Napa County agricultural areas (2006) tions. UC scientists evaluated the efficacy 80 and longevity of four pheromone lures in replicated field experiments in Napa Fig. 1. The state interior quarantine established in Napa County, California, following the first detection during the first and second moth flights of EGVM (September 29, 2009) in North America. The area encompassed all areas within a 5-mile (8 km) of 2010 (Varela et al. 2013b). All lures were radius of all known EGVM populations at that time, as determined by trap captures and ground surveys.

TABLE 2. Quarantine area in square miles (vineyard acres inside quarantine) by county and year

San Year Napa Sonoma Solano Mendocino Fresno Merced Joaquin Santa Cruz Santa Clara Nevada California total ...... Square miles (vineyard acres) ...... 2010 597 664 237 179 96 108 96 0 94 0 2,091 (43,139) (52,000) (2,397) (5,860) (24,769) (1,432) (20,544) (0) (619) (0) (150,760) 2011 597 664 237 179 96 108 96 87 94 176 2,335 (43,452) (52,000) (2,397) (5,860) (24,769) (1,432) (20,544) (310) (619) (345) (151,728) 2012 575 458 124 34 38 74 1,302 (43,078) (46,500) (2,289) (231) (552) (99) (92,749) 2013 554 78* 55† 687 Removed from quarantine 3/8/2012 (42,703) (5,600) (1,009) Removed from quarantine (49,312) 2014 554 78 55 12/21/2012 687‡ (42,703) (5,600) (1,009) (49,312) * In Sonoma County, 380 square miles were removed from quarantine on 12/21/2012. † In Solano County, 69 square miles were removed from quarantine on 8/24/2012. ‡ Effective August 2014: the quarantine area measures 446 square miles, following the removal of Solano County and portions of Napa and Sonoma counties.

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 127 Glenn Sierra Butte effective for monitoring EGVM male moth Mendocino Nevada populations during and beyond the pe- Colusa riod recommended by the manufacturer Yuba Placer Lake Sutter (fig. 3). International technical working group In November 2009, USDA assembled Yolo El Dorado a technical working group (TWG) of Sonoma Napa Alpine subject-matter experts to provide urgent Sacramento scientific recommendations to regulatory Amador program managers in California. The Solano Mono TWG included university scientists from Calaveras Italy, France, Germany, Spain, Chile and Marin Tuolumne California, as well as USDA scientists Contra Costa San Joaquin (and chair) and a representative of the San Francisco wine grape industry. TWG members con- tinue to meet annually to review program Alameda activities and provide technical expertise Stanislaus Mariposa San Mateo on topics as diverse as insect biology, de- tection strategies, handling of harvested Santa Clara fruit and winery waste, and management Merced activities. Santa Cruz Madera Since 2010, TWG members have agreed that eradication of EGVM from California remains a realistic goal as long as (1) the population did not become substantially EGVM quarantine areas San more widespread than was known at that 8/25/2014 (446 square miles) Benito time, (2) the grape industry remained 2013 (686 square miles) Fresno supportive of the effort and (3) effec- 8/21/2012 (1,234 square miles) tive control methods were available for 6/13/2011 (2,335 square miles) Monterey use by the program (Mastro et al. 2010). 9/20/2010 (2,091 square miles) Over the course of the EGVM program, Kings Tulare 11/16/2009 (162 square miles) TWG members evaluated research data Vineyards and program developments to formulate recommendations based on the insect’s San Luis Obispo Kern biology. Government agencies matched Fig. 2. Regulated areas of California for EGVM, defined by USDA, 2009 to 2014. these recommendations to political and fiscal analyses to formulate and deliver the EGVM program.

Craig Graffin Craig Management tools Treatment areas. Treatment areas were defined within a requisite distance from all detections and included agricultural, residential and commercial properties. In 2010, the distance was not standardized, so the size of the treatment areas varied by county. Following a review of the sci- entific literature suggesting that EGVM are short-distance fliers, the TWG recom- mended a treatment area within 1,640 feet (500 meters [m]) of all detections regard- less of when the detection occurred. From 2013 onward, the TWG modified this recommendation to account for timing of the detection: Treatment areas came to be defined as within 500 m of detections occurring in the current year and previ- The distinctive color pattern on EGVM wings make them easily recognizable in pheromone-baited traps. ous 2 years. Within the treatment areas,

128 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 grape and olive were the targeted hosts 500 of concern, and total vineyard acreage 450 Alpha Scents varied considerably by county and year USDA (table 3). The specific combination of tools 400 Trece (insecticides, mating disruption and host Suterra removal) used in treatment areas differed 350 by land use and occurrence of potential B B B A host plant species. 300 Changed: Insecticide program. The recom- Alpha Scents mended insecticide program for EGVM in 250 Trece California vineyards targets the eggs and larvae and includes at least one applica- 200 tion of a conventional insecticide or at least two applications of an organic insec- 150

ticide for each of the first two generations Average no. male moths/trap/week (and for the third generation in extenuat- 100 B B B A ing circumstances). Although treatment 50 A AB A A of the first generation is not typical in the

Palearctic regions, the TWG determined 0 that treating the first two generations in Mar 4 Mar 11 Mar 18 Mar 25 Apr 1 Apr 8 Apr 15 Apr 22 California would provide the greatest opportunity to eradicate populations. In Fig. 3. Average number of male moths caught in traps baited with commercial pheromone lures and a early 2010, UC scientists provided an ex- USDA lure monitored from February 25 to April 22, 2010. Alpha Scents, USDA and Trece lures are rubber haustive list of potential insecticides for septa, and Suterra is a membrane lure. Letters indicate homogenous groups at 95% least significant difference. Per the manufacturer’s recommendation, the Alpha Scents and Trece lures were changed 4 EGVM management based on a review weeks into the experiment. of the scientific literature. From this list, EGVM program leaders made a concerted Chlorantraniliprole, methoxyfenozide, each life stage (Caffarelli and Vita 1988; effort to identify and recommend prod- spinosad and Bacillus thuringiensis pro- Touzeau 1981). Referencing these observa- ucts that would provide selective control vided control of young larvae; abamectin, tions and calculations to local weather of EGVM while minimizing risks to non- indoxacarb and spinetoram provided data and vine phenology, UC scientists target organisms and the environment. the best control of mature larvae (Van then determined the optimal timing for The availability of organic treatment Steenwyk et al. 2011). These results were insecticide applications for all affected options ensured that growers could main- widely distributed to the program team locations in California. For each genera- tain organic certification while complying and grape growers. tion, a 3-week treatment window mini- with the eradication effort. Pesticide use Insecticide treatment. Selective insec- mized application costs by combining the reporting (PUR) data for Napa County ticides are most effective if applied when insecticide with preventative treatments (2010 to 2014) indicate that growers used a the pest is at its most susceptible stage for powdery mildew. This information combination of the recommended materi- (Ioriatti et al. 2011). In Napa County, UC was widely disseminated via conference als (table 4). scientists monitored the male flight, egg calls with government agencies, a UC Insecticide efficacy trials. UC scientists and larva development and calculated electronic newsletter, industry associa- conducted field trials in commercial vine- degree-days (lower and upper thresh- tions’ e-news blasts, and grower liaisons yards in Napa in 2010 to evaluate the effi- olds of 50°F and 86°F [10°C and 30°C], in Napa, Sonoma, Fresno and Mendocino cacy of registered insecticides for EGVM. respectively) from a biofix of January 1 for counties. An analysis of the PUR data

TABLE 3. Insecticide-treated acres and reported use of Isomate EGVM pheromone dispensers in counties affected by quarantine regulations

Year Napa Sonoma Solano Mendocino Fresno Merced San Joaquin Santa Cruz Santa Clara Nevada ...... Insecticide-treated acres (acres under mating disruption) ...... 2010* ~8,000 594 94 928 620 364 N/A N/A N/A (0) (0) (13) (0) (0) (0) 2011† 23,700 2,395 785 201 540 200 83 16 114 8 (13,300) (1,533) (0) (100) (0) (0) (0) (0) (0) (8) 2012‡ 28,000 2,395 N/A N/A N/A N/A N/A 16 114 8 (23,071) (0) (0) (0) (0) 2013§ 11,800 23 N/A N/A N/A N/A N/A N/A N/A N/A (2,800) (0) * Treatment areas are within 1,000 m of any detection in 2010 (except Napa and Solano [200 m]). † Treatment areas are within 500 m of any detection in 2010 or 2011. ‡ Treatment areas are within 500 m of any detection in 2010, 2011 or 2012. § Treatment acres are within 500 m of any detection in 2011, 2012 or 2013.

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 129 from 2011 and 2012 shows a high level of regions, MD has provided sustained con- supported the use of MD as a control tool compliance for treatment timing among trol of EGVM populations while decreas- (Ioriatti et al. 2004; Lucchi et al. 2012), Napa County growers (table 5). ing reliance on insecticides and reducing and by the second EGVM flight of 2010, Mating disruption. Mating disruption conflict between agricultural and urban Isomate EGVM pheromone dispensers (MD) programs deploy synthetic (E,Z)- populations (Ioriatti et al. 2011). Although (Pacific Biocontrol, Vancouver, WA) be- 7,9-dodecadienyl acetate — the main MD does not completely inhibit EGVM came widely used (table 3). component of the female sex pheromone mating, delayed mating reduces popu- After the MD and insecticide pro- — in hand-applied dispensers (Pasquier lations because older females produce grams were implemented, trap catches and Charmillot 2005). When applied as fewer eggs than younger females (Torres- and visual inspections revealed dramatic an area-wide control strategy in Palearctic Vila et al. 2002). TWG scientists strongly decreases in population size in Napa County (table 1). Beginning in 2012, all TABLE 4. Pesticide use report data collected by the Napa County agricultural commissioner for Napa County vineyards within the de- applications targeting EGVM during the first and second generations of 2011 and 2012 within defined fined treatment areas received pheromone treatment areas (all vineyards within 500 m of all EGVM detections) dispensers through federal, state and lo- First Second Percent of Percent of cal funding programs. Because MD limits generation generation Year Acres treated total acres Sites treated total sites the reliability of sex pheromone–baited Conventional Conventional 2011 11,111 46.9 593 48.4 traps and makes it very difficult to detect 2012 11,597 60.9 444 52.5 residual populations, the EGVM program has avoided the use of MD in treatment Organic Organic 2011 2,073 8.7 113 9.2 areas as they transition to deregulation. 2012 2,492 13.0 115 14.0 Urban and residential treatment pro- Conventional Conventional 2011 41 0.17 4 0.33 grams. CDFA personnel used multiple or organic or organic strategies to manage EGVM populations 2012 195 1.0 15 1.8 in noncommercial grapevines in urban Insecticide None 2011 5,290 22.3 194 15.8 and residential areas. The organic product 2012 1,063 5.6 83 9.8 B. thuringiensis was applied during the first and second generations if the crop None Insecticide 2011 1,783 7.5 73 6.0 was to be harvested; if not, flower and/or 2012 814 4.3 51 6.0 fruit clusters were removed in the spring None None 2011 3,399 14.3 249 20.3 or early summer (table 6). MD was also used in certain areas and select counties. 2012 2,869 15.1 138 16.3

Conventional insecticides: abamectin, chlorantraniliprole, and methoxyfenozide; organic insecticides: spinosad and Bacillus thuringiensis. Alternate host surveys “None” indicates that no insecticide targeting EGVM was reported. Polyphagy by EGVM has been docu- mented in the literature: Larvae may TABLE 5. Timing of reported insecticide treatments in Napa County targeting the first and second generations of 2011 and 2012 categorized as: recommended timing, before or after feed on up to 40 hosts in 27 plant families (Ioriatti et al. 2011; Lucchi and Santini Acres treated, by treatment timing Acres treated, by treatment timing 2011). However, larvae are rarely found on for first generation for second generation (percent of total) (percent of total) hosts other than Daphne gnidium and Vitis; exceptions seem to result from adapta- Product Year Before Recommended After Before Recommended After tions to local climate and flora (Ioriatti Chlorantraniliprole 2011 — 444 65 1,109 9,639 68 (Altacor) (87) (13) (10) (89) (1) et al. 2011) or elevated pest pressure and 2012 — 2,803 286 989 6,254 2,072 presence of ripe fruit (Maher 2002). UC (91) (9) (11) (67) (22) and USDA personnel used pheromone- Methoxyfenozide 2011 3 13,085 1,558 165 1,432 7 baited traps and visual surveys to monitor (Intrepid) (< 1) (90) (10) (10) (89) (< 1) a variety of plant species in Napa County 2012 299 11,771 1,606 181 2,853 1,509 that are reported to be EGVM hosts (2) (86) (12) (4) (63) (33) (table 7); no EGVM life stages were found Bacillus 2011 0.3 2,752 195 225 1,968 35 during these surveys, suggesting that thuringiensis (< 1) (93) (7) (10) (88) (2) these species currently pose little risk in and/or spinosad 2012 210 3,146 346 745 2,464 152 California. In separate surveys of olive (6) (85) (9) (22) (73) (5) orchards, 10 eggs and 12 EGVM larvae Abamectin 2011 — 66 8 — 324 — were found, indicating that olive flowers (Agri-Mek) (89) (11) (100) were a minor host in Napa during the 2012 12 110 — 16 23 — first EGVM generation, but olive fruit (9) (91) (41) (59) did not host the second or third genera- Flubendiamide 2011 — — — — — — tions. The main host of consequence in 2012 — — 91 540 — — California continues to be cultivated (14) (86) grape, Vitis vinifera.

130 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 TABLE 6. Treatments for EGVM in noncommercial grapevines in urban areas included flower/fruit removal, applications of Bacillus thuringiensis (Bt) and mating disruption (MD)

Number of properties by California county Year Treatment Fresno Mendocino Merced Napa Nevada San Joaquin Santa Clara Santa Cruz Solano Sonoma 2010 Fruit removal 24 168 1 7 115 Bt 2 1 1 2011 Fruit removal 23 148 1 189 1 9 14 306 165 Bt 7 42 1 12 13 4 63 34 MD 2,651 601 2012 Fruit removal 112 8 11 294 200 Bt 36 14 6 75 147 MD 860 2013 Fruit removal 157 Bt 121 MD 373

Compliance agreements TABLE 7. Surveys of alternate host plants along washing of all equipment used to harvest, the Napa River, 2010–2011 To prevent the movement of EGVM transport and process infested loads of on regulated articles grown inside quar- grapes. Plant type Number of fruit/flowers inspected antine areas, CDFA required businesses Blackberry 55,625 Outreach and educational program to sign compliance agreements that Elderberry 230,615 mandated specific activities prior to and EGVM program leaders provided Olive 3,937 (and 4,837 leaves) during harvest, transport, processing and transparent, consistent, timely and co- Wild rose 2,962 waste handling. Compliance agreements ordinated communication to parties Wild or 28,471 were also required for similar activities directly and indirectly affected by the domestic grape in raisins and regulated fruit other than EGVM program. USDA led international Wild or 2,582 grape, including olive, persimmon, pome- communications and jointly with CDFA domestic plum granate, most stone fruit (Prunus spp.) coordinated statewide communication. Peach 83 and specific caneberries. Based on recom- County agricultural commissioners and Nectarine 83 mendations provided by the TWG, in 2012 UC advisors directed local communica- Walnut 226 the USDA revised the list of regulated tion and assisted in other efforts. The Blueberry 305 articles to exempt olive fruit and Rubus outreach program also collected relevant Gooseberry 342 spp., and limited the acreage of Prunus information from stakeholders to ensure spp. affected. the appropriateness of regulatory require- ments and adapted the program to local information. The online UC IPM Pest Management of winery waste conditions and concerns. This openness Alert presented information on pest iden- The possibility that EGVM could sur- and flexibility to change fostered the tification, biology and management. vive in unfermented winery waste was development of trust, respect and coop- Grower liaison/outreach coordina- addressed by requiring that waste be eration among all parties. The proactive, tors in Napa, Sonoma, Mendocino and composted on site, transported to an ap- local campaign to communicate, educate Fresno counties played an important role proved compost facility or returned to the and collaborate with a diverse community in outreach and educational efforts. In vineyard of origin, depending on where became a hallmark of the EGVM program each county, the EGVM grower liaison the fruit was sourced relative to the quar- (Zalom et al. 2013). conducted targeted outreach and was a antine area and county. Alternatively, if Industry outreach and education. Many trusted, independent source of informa- grapes were pressed to a minimum of 2 methods were used to communicate tion for growers and winery personnel. bars (0.2 MPa) or 28 psi, then movement of information to growers and winery per- Program information was communicated waste was unrestricted within California. sonnel. Educational materials included at meetings, seminars and field days, as Investigations provided evidence that two tri-fold brochures, a poster and well as through individual communica- EGVM larvae could survive on unpressed training videos developed and distrib- tions and a UC Cooperative Extension green waste after destemming and de- uted through UC Cooperative Extension. Napa County newsletter. Farmworkers — termined that in general the processing Mass marketing campaigns raised public particularly important “first responders” equipment was likely a greater source of awareness using postcards, door-hangers, capable of identifying potential threats contamination than unfermented waste magnets, billboards and campaign signs, during their daily work — were reached (Smith et al. 2013). Mature larvae may public service announcements, and online through Spanish language presenta- move from clusters to protected loca- and social media; cross-linked websites tions, field days and outreach materials. tions, emphasizing the need for thorough provided comprehensive and current Partnerships with local industry groups

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 131 et al. 2012). Any moth captured will trig- ger the delimitation and establishment of treatment areas within 1,640 feet (500 m) of the detection. Consequently, trap density nearly tripled in Napa County in 2013 (table 1) and the area under MD shrank from 23,000 to 2,800 acres in 2013 and approximately 1,907 acres in 2014. The remaining EGVM population in Napa County has been drastically reduced in size and distribution (fig. 2; table 1). By mid-August 2014, southern Sonoma County, the remainder of Solano County, and a portion of southern Napa County were removed from quarantine. The re- mainder of Napa County and a portion of northern Sonoma County, an area total- ing 446 square miles, will continue to be regulated in 2015. Pheromone-baited trap surveys continue in other grape-growing areas of California and the United States as part of CDFA/USDA early detection programs. These surveys detected one moth in Sonoma County in 2014; this was not sufficient to trigger establishment of a Emily Kuhn new quarantine boundary. The public campaign “Kick the Moth Out” raised awareness of the EGVM program in Napa County. A model collaborative effort to deliver program information contrib- second generation, (3) MD may not be Development and implementation uted to the educational efforts. Growers used during the final two generations that of a successful regulatory program in also shared information and related their the area is under regulation and (4) dur- response to the detection of an invasive experiences through peer networks that ing these two generations, trap density species in California agricultural systems strengthened the formal educational must increase to 100 traps per square mile requires a concerted and coordinated ef- program. (39 traps per km2) (one trap per 6 acres) fort to address the pest while balancing Public outreach and education. An in all vineyards within 1,640 feet (500 m) the needs of the agricultural industry, estimated 2.5 million acres of California of previous detections. Under California trading partners and the general public. farmland are adjacent or in close proxim- conditions, only the first and second are Regulatory, fiscal, environmental and ity to nonfarm residences (Hammond considered full generations because a pro- biological aspects must be weighed to et al. 2010). To address potential areas of portion of the second generation enters develop goals and determine program urban-agricultural conflict, county ag- diapause (L. Varela and M. Cooper, per- activities. The leaders of the California ricultural commissioners supported by sonal observation). Four counties (Fresno, EGVM program were sensitive to these USDA, CDFA, UC and industry groups Mendocino, Merced and San Joaquin) issues and gained credibility and trust worked within established local networks were removed from regulation at the be- by involving a diverse community for of community leaders to develop a public ginning of 2012, and by the end of 2012, dialogue, responding to the needs of local outreach campaign. County supervisors five additional counties (Nevada, Santa communities, considering the impact on and city council members, environmental, Clara, Santa Cruz, Solano and Sonoma) the environment, adopting new scientific community and commercial organiza- had been deregulated partially or in full. information, investing in relationships tions, residents and tourists were the Napa County and portions of neigh- and networks, and ensuring the appro- targets of the outreach efforts, which built boring Sonoma and Solano counties re- priateness of regulatory requirements trust between program and community mained under regulation in 2013, an area (Zalom et al. 2013). Factors such as the leaders, growers and the public. encompassing 686 square miles (fig. 2). insect’s limited host range, which allowed Due to the historically large and widely the program to focus on commercial vine- Program update distributed populations in Napa County, yards; the use of management tools that The conditions set forth by the TWG the TWG recommended a revised ap- minimized the impact to nontarget organ- specified that in areas attempting to proach to deregulation: High-density isms and are compatible with organic and qualify for deregulation (1) no moths traps (100 per square mile) deployed backyard vineyards; and the long history must be captured during five consecutive county-wide must be free from detections of EGVM management in the Palearctic generations, (2) insecticide treatments during four full flights before areas will region also contributed to the successes must continue to target the first and be considered for deregulation (Mastro of the program. The EGVM program

132 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 leaders were recognized with the USDA Administrator’s Award in September 2012, acknowledging the program’s suc- cessful collaborative approach. The pro- gram has clear direction and well-defined goals, is grounded in biology, engages a diverse community and is responsive to the changing needs of participants. The participation of USDA, CDFA, agricultural commissioners, UC and other university scientists, growers, industry groups, com- munity leaders and the general public re- sulted in a model effort that has reduced EGVM populations to a few areas of Napa and Sonoma counties. c

M. Cooper is UC Cooperative Extension (UCCE) Farm Advisor-Viticulture, Napa County; L. Varela is UCCE IPM Advisor-North Coast; R. Smith is UCCE Farm Advisor-Viticulture, Sonoma County; D. Whitmer is Agricultural Commissioner and Sealer of Weights & Measures (Retired), Napa County; G. Simmons is CPHST Supervisory Agriculturist, USDA, APHIS, PPQ; A. Lucchi is Professor, University of Pisa, Italy; R. Broadway is GIS Specialist, USDA, APHIS, PPQ; and R. Steinhauer is Wine Grape Grower, Wineland Consulting, Napa, CA. Emily Smith

Field day training sessions with growers and farmworkers were held in Oakville, CA, in April 2010.

References Boller EF. 1993. Wie weit fliegt der Traubenwickler? Deut. Lucchi A, Bagnoli B, Cooper M, et al. 2012. The successful Smith RJ, Cooper ML, Varela LG. 2013. Determining the Winbau Jahrbuch 44, Waldkircher Verlag, Waldkirch, use of sex pheromones to monitor and disrupt mating of threat of dispersal of Lobesia botrana larvae in infested Germany. Lobesia botrana in California. Working group meeting on grapes processed for winemaking. Practical Winery and Caffarelli V, Vita G. 1988. Heat accumulation for timing pheromones and other semio-chemicals in integrated Vineyard August 2013:73. grapevine moth control measures. Bulletin SROP 11:24–6. production, October 1–5, 2012, Bursa, Turkey. IOBC-WPRS Torres-Vila LM, Rodríguez-Molina MC, Stockel J. 2002. Bulletin 99:45–8. [CDFA] California Department of Food and Agriculture. Delayed mating reduces reproductive output of female 2012. European grapevine moth (Lobesia botrana) state Lucchi A, Santini L. 2011. Life history of Lobesia botrana European grapevine moth, Lobesia botrana (Lepidoptera: interior quarantine. In: California Department of Food on Daphne gnidium in a natural park of Tuscany. IOBC- Tortricidae). B Entomol Res 92:241–9. and Agriculture Plant Quarantine Manual 3437:422.1–12. WPRS Bulletin 67:197–202. Touzeau J. 1981. Modelisation de l’evolution de l’Eudémis http://pi.cdfa.ca.gov/pqm/manual/pdf/422.pdf. Maher N. 2002. Oviposition site selection by Lobesia de la vigne pour la région Midi-Pyrenées. Bol Zool Agr Gutierrez AP, Ponti L, Cooper ML, et al. 2012. Prospective botrana (Lepidoptera: Tortricidae): Influence of non- vola- Bach II 16:26–8. analysis of the invasive potential of the European grape- tile chemical cues from host plants fruits [in French]. PhD USDA. US Department of Agriculture. 2010. Establish- vine moth Lobesia botrana (Den. & Schiff.) in California. thesis, Université de Bordeaux 2, France. 109 p. ment of Quarantine Areas in California for European Agr Forest Entomol 14:225–38. Mastro V, Cardé R, Cooper M, et al. 2012. Report of the Grapevine Moth, Lobesia botrana. APHIS Federal Do- Hammond SV, Norton MV, Schmidt EE, Sokolow A. 2010. Technical Working Group for the European Grapevine mestic Quarantine Order DA-2010-25, June 22, 2010. 6 California communities deal with conflict and adjust- Moth Program in California. October 30-November 1, p. www.aphis.usda.gov/plant_health/plant_pest_info/ ment at the urban-agricultural edge. Calif Agr 64:121–8. 2012, Sacramento, CA. www.aphis.usda.gov/plant_ eg_moth/downloads/spro/DA-2010-25.pdf. doi: 10.3733/ca.v064n03p121. health/plant_pest_info/eg_moth/downloads/TWG- Van Steenwyk RA, Varela LG, Cooper ML. 2011. Monitor- Report-Dec2012.pdf. Ioriatti C, Anfora G, Tasin M, et al. 2011. Chemical ecology ing and control of European grapevine moth, Lobesia and management of Lobesia botrana (Lepidoptera: Tor- Mastro V, Cardé R, Lance D, et al. 2010. Second Report of botrana (Lepidoptera: Tortricidae) in California vineyards. tricidae). J Econ Entomol 104:1125–37. the USDA International Technical Working Group for the Abstracts of the IOBC-WRPS meeting in Lacanau, France. European Grapevine Moth in California. May 14, 2010. October 2–5, 2011. Ioriatti C, Bagnoli B, Lucchi A, et al. 2004. Vine moths www.aphis.usda.gov/plant_health/plant_pest_info/ Varela LG, Cooper ML, Smith RJ. 2013a. Can European control by mating disruption in Italy: Results and future eg_moth/downloads/TWG%20report-5-14-2010.pdf. prospects. REDIA 87:117–28. grapevine moth, Lobesia botrana (Lepidoptera: Tortric- Pasquier D, Charmillot PJ. 2005. Survey of pheromone idae) be eradicated from California? In: Calonnec A, Duso Ioriatti C, Lucchi A, Varela LG. 2012. Grape berry moths in emission from different kinds of dispensers used for C, Gessler C, et al. (eds.). IOBC/WPRS Bulletin 85:92–102. western European vineyards and their recent movement mating disruption in orchards and vineyards. IOBC-WPRS Varela LG, Cooper ML, Smith RJ. 2013b. Trapping for Euro- into the New World. In: Bostanian NJ, Vincent C, Isaacs Bulletin 28:335–40. R (eds.). Arthropod Management in Vineyards: Pests, pean grapevine moth. CAPCA Adviser 16:20–5. Approaches, and Future Directions. Springer Science + Schmitz V, Roehrich R, Stockel J. 1996. Dispersal of Zalom F, Grieshop J, Lelea M, et al. 2013. Community Business Media B.V. p 339–59. doi: 10.1007/978-94-007- marked and released adults of Lobesia botrana in an iso- Perceptions of Emergency Responses to Invasive Species 4032-7_14. lated vineyard and the effect of synthetic sex pheromone in California: Case Studies of the Light Brown Apple Moth on moth movements. J Int Sci Vigne Vin 30: 67–72. and the European Grapevine Moth. Report submitted to USDA in fulfillment of Cooperative Agreement #10-8100- 1531-CA.

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 133 MANAGING NEWLY ESTABLISHED PESTS AND DISEASES

Cooperative efforts contained spread of Pierce’s disease and found genetic resistance by George Bruening, Bruce C. Kirkpatrick, Thomas Esser and Robert K. Webster

An outbreak of Pierce’s disease of grapevine in the Temecula Valley in the late 1990s ierce’s disease (PD) was not new was one in a decades-long series of sporadic appearances of this infection in California. to California in 1999, when its characteristic scorching symptoms However, the new outbreak was qualitatively different because of the rapidity with P suddenly and severely devastated several which it spread in the vineyard and its appearance almost simultaneously at distant hundred acres of grapevines in the Tem- locations. The causative agent of Pierce’s disease is the bacterium Xylella fastidiosa, ecula Valley, affecting a quarter of the and the distinct characteristics of the Temecula Valley outbreak were traced to the region’s vineyards. In the early 1880s, PD, then referred to as Anaheim disease, deci- establishment of a new insect vector in California, the glassy-winged sharpshooter. mated 30,000 acres of vines near Anaheim Intensive and collaborative efforts among government agencies, industry and research and Pomona. Newton B. Pierce, a special institutions over 15 years have successfully contained the disease, and given scientists agent of the U.S. Secretary of Agriculture, time to discover promising long-term potential solutions through genetic resistance. responded to this event as the first profes- sional plant pathologist in California. He skillfully eliminated explanations other than disease but was not able to identify the causative agent. In the late 1880s,

Jack Kelly Clark Jack Kelly the disease damaged vineyards in Napa County, and there were severe outbreaks in Southern California in the 1930s and 1940s. Between 1994 and 2000, grapevines on over 1,000 acres in Northern California were affected, resulting in $30 million in damage (Webster and Nation 2000). The causative agent of PD was long thought to be a virus. The disease actu- ally is caused by a strain of the bacterium Xylella fastidiosa (Davis et al. 1978). Strains of this bacterium also inflict damage on many other plant species, including al- mond, citrus, elm, maple, oak, oleander, stone fruit and sycamore. The 1999 out- break in the Temecula Valley was unique, alarming and characterized by rapid and long-distance spread of PD in the vine- yard, resulting from the establishment of a new vector in California, the glassy- winged sharpshooter (GWSS; Homalodisca vitripennis). Further spread of GWSS would place at risk California’s $3 billion grape crop, $60 billion in associated activ- ity, and $3 billion in fruit, nut and orna- mental crops. Epidemiology of PD X. fastidiosa is transmitted in the field by xylem-feeding insects, especially

Online: http://californiaagriculture.ucanr.edu/ PD symptoms on a red grape variety, showing progressive foliage discoloration, irregular bark maturity and petioles without leaf blades. The Temecula Valley PD outbreak in 1999 triggered an landingpage.cfm?article=ca.v068n04p134&fulltext=yes emergency response to save the wine and grape industries. doi: 10.3733/ca.v068n04p134

134 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 sharpshooters (family Cicadellidae, sub- quickly than others (Hopkins and Purcell family Cicadellinae) and related insects 2002). Muscadine varieties (V. rotundifoli a) such as spittlebugs (family Cercopidae) and certain Vitis hybrids, especially those (Hopkins and Purcell 2002). Insect vec- that are endemic to North America, such tors acquire X. fastidiosa from infected as V. labrusca X V. vinifera (Concord grape), plants; some plants are much more effec- support only very low X. fastidiosa titers, tive sources of the bacterium than others, which do not affect fruit quality or kill depending on vector feeding preferences the vine. and patterns of X. fastidiosa accumula- The incidence and severity of PD in tion and spread in the plant (Purcell and California vineyards have been cyclic Saunders 1999). Ingested X. fastidiosa at- since the first record of PD in Anaheim taches to the sharpshooter’s mouthparts, and Pomona in the early 1880s. A PD epi- where it multiplies. Transmission to demic occurred from 1933 to 1940 in the healthy plants occurs when the infected Central Valley, where diseased vineyards vector feeds and egests the bacterium were often located next to weedy alfalfa into the plant’s xylem. Plant symptoms, fields, which were breeding sites for green if any, appear weeks to months later. All (Draeculacephala minerva) and red-headed Clark Jack Kelly GWSS adults caught in a yellow sticky trap. In nymphal stages of the sharpshooter can (Xyphon fulgida) sharpshooters (Hopkins areas infested with GWSS, trap counts indicate acquire X. fastidiosa, but nymphs lose the and Purcell 2002). The blue-green sharp- when insecticides should be applied to citrus bacterium when they molt, because the shooter (BGSS; Graphocephala atropunctata), groves located near vineyards. mouth lining is shed during molting. If a very efficient vector of PD, was largely the sharpshooter acquires X. fastidiosa responsible for the severe outbreaks of PD economically important pest of grape- as an adult, it remains infective for the that have occurred in the coastal regions vines in its own right (Andersen et al. remainder of its life (Hopkins and Purcell of Northern and Southern California and 2003), its establishment greatly increased 2002; Purcell and Finley 1979). in the interior areas of Napa and Sonoma the incidence and severity of PD in the PD is most prevalent in grape-growing counties (Redak et al. 2004; Webster and viticultural regions of Southern California regions of the Southern U.S. states, Mexico Nation 2000). and the lower San Joaquin Valley. To date, and Central America, in areas that have None of these sharpshooters is a strong GWSS has not become permanently estab- mild winter temperatures. Research has flyer, so the PD infections they cause are lished north of Fresno County, although shown that Vitis vinifera vines experi- typically limited to an area of a few hun- incipient infestations have occurred mentally infected with X. fastidiosa will dred meters from their overwintering sporadically and have been successfully become pathogen-free if the vines are sites, which for the BGSS are weedy ripar- eradicated thus far (CDFA 2013). subjected to cold temperatures (Feil and ian areas and ornamental landscapes. The epidemiology of PD transmitted Purcell 2001; Lieth et al. 2011). This cold Vineyards can be protected by treating by GWSS differs considerably from the curing phenomenon likely accounts for them with insecticides in the spring in epidemiology of PD spread by the BGSS the lack of PD in viticultural regions such response to BGSS counts in yellow sticky and other native sharpshooters. GWSS, as New York, Oregon, Washington and panel traps (Varela et al. 2001). When surprisingly, is a less efficient vector of higher-elevation vineyards in California, the emerging shoots are short, BGSS- where vines experience cold winter tem- vectored X. fastidiosa can reach the per- GWSS flies farther than other sharpshooters, peratures. A recent model based on cold manent woody tissues of the vines and has a polyphagous diet and can spread PD vine curing data by UC Davis professor Johan cause PD that persists and kills the vines. to vine. It initiates infections on a nearly year- Lieth showed good predictive correlations Inoculation of the green tips of longer round basis. between winter temperatures and the canes later in the season tends to not presence or absence of PD in viticultural result in systemic disease, since regions in California (Lieth et al. 2011). the infected portions of the Global warming is expected to alter crop vines are pruned off (Feil geographical distributions (Weare 2009) et al. 2003). and could reduce the areas currently sub- The glassy-winged ject to cold curing. Where winter tempera- sharpshooter tures have warmed in the Southeastern states, PD distribution has increased GWSS probably (Anas et al. 2008). entered Southern All cultivars of European grapevine, California on im- V. vinifera, are susceptible to X. fastidiosa ported plant material infection. While most varieties eventu- in the late 1980s or ally die from the infection, some varieties early 1990s. While GWSS Jack Kelly Clark are more susceptible and succumb more is not considered to be an

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 135 X. fastidiosa than native California sharp- shooters (Daugherty and Almeida 2009). However, GWSS is a highly polyphagous insect, feeding on a variety of plants to fulfill its nutritional requirements (Varela et al. 2001). It also flies much greater distances than the native sharpshooters. The severe PD losses that occurred in the Temecula region in the late 1990s and early 2000s often occurred in vineyards located adjacent to citrus orchards, which are preferred feeding and breeding hosts of GWSS. PD transmitted by GWSS can rapidly encompass an entire vineyard, Clark Jack Kelly During hot weather, PD causes leaves to turn brown, typically first at the leaf margins. New infestations and significant PD losses occurred in are met with a rapid response and have been eradicated in Northern California counties. vineyards located a mile or more from citrus orchards. regulations required inspection, treat- implemented in other infested viticultural Unlike native PD vectors, GWSS can ment, monitoring and certification of ship- areas. Removal of diseased vines helped acquire and transmit X. fastidiosa from ments from infested areas. Enforcement reduce the incidence and sources of dis- woody tissues such as 1- to 2-year-old of the regulations is coordinated by the ease in these areas. lignified canes (Almeida and Purcell CDFA and usually performed by the staff Detection. In addition to the GWSS 2003; Almeida et al. 2005), and even spurs of county agricultural commissioners containment activities, annual detection that remain when the dormant vines (CDFA 2001). surveys in agricultural and urban areas are pruned. Thus, The certification program, established were begun to search for new GWSS in- GWSS spreads to ensure that shipments of nursery stock festations and verify that uninfested areas See also: Jetter KM, X. fastidiosa on a were free of GWSS, was effective but remained free of GWSS. Surveys rely Morse JG, Kabashima nearly year-round proved to be labor intensive, expensive primarily on sticky yellow panel traps JN. 2014. The cost of basis and initiates and a significant burden to many grow- deployed in areas deemed at risk of GWSS the glassy-winged chronic infections ers (Redak and Bethke 2003). In response, introduction. Trapping is conducted every sharpshooter to Cali- of vines. Extensive concerted efforts were made to find a year during the warm-weather months, fornia grape, citrus and disease map- treatment that could be relied upon to with some locations being monitored nursery producers. ping done in the minimize the risk of spreading GWSS on year-round. Calif Agr 68(4): 161-167. early stages of the shipments of plant material from infested Rapid response. Discovery of one or http://california Temecula epidemic areas. While adult and nymphal GWSS more GWSS in a new area triggers rapid agriculture.ucanr.edu/ showed that GWSS were found to be fairly susceptible to response activity by the CDFA, which landingpage.cfm? can spread X. fas- insecticide treatments, the egg masses consists of intensive visual survey and article=ca.E.v068n04 tidiosa vine to vine. of the insect, embedded in the foliage deployment of more traps to determine if p161&fulltext=yes Other PD vectors of plants, were not (Grafton-Cardwell et a new infestation exists and, if so, where tend to introduce al. 2003; Redak and Bethke 2003). Trials its boundaries lie. New infestations are the bacterium from conducted by researchers at UC Riverside treated with insecticides applied primar- infected nongrape- eventually identified two insecticides ef- ily to preferred host plants of GWSS to vine sources outside the vineyard rather fective against all GWSS stages. Based on eradicate the infestation (CDFA 2013). than from chronically infected vines the trial results and beginning in 2008, Outreach. Outreach plays an important (Varela et al. 2001). the Nursery Stock Approved Treatment role in GWSS containment and suppres- Protocol (Kabashima et al. 2011) became sion efforts. Outreach activities, including Preventing spread of GWSS an optional substitute for the certification meetings, mailings and media pieces pre- After the magnitude of the threat from program. pared by CDFA, UC, counties and outside the Temecula PD epidemic was realized, In large grape production areas that contractors, are aimed at the affected in- the California Department of Food and were already infested with GWSS, such dustries and the general public to inform Agriculture (CDFA) put in place a success- as portions of Kern, Riverside and Tulare them of the new pest threat in California ful four-pronged program: containment, counties, area-wide trapping and treat- and the new programs and activities be- detection, rapid response and outreach. ment programs for reducing GWSS num- ing conducted to address it. These efforts Containment. Within the infected ar- bers were implemented and evaluated. In have helped gain compliance with new eas, the CDFA promulgated regulations these programs, coordinated insecticide shipping requirements and enlisted assis- aimed at interdicting likely pathways treatments were applied primarily to tance from the public in finding new in- of GWSS spread from infested areas of citrus and, on occasion, to windbreaks, festations and preventing further spread Southern California. This involved regu- when trap counts revealed GWSS popu- of GWSS. lating shipments of general nursery stock, lations at or above damage thresholds Success of the current four- bulk grapes and (later) bulk citrus. The (CDFA 2005). Similar programs were later pronged program is evidenced by two

136 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 observations: The GWSS-infested area in being conducted on an ongoing basis collected in the Southern U.S. states and California this year is only slightly larger (CDFA 2001, 2013). northern Mexico (Walker and Riaz 2012). than the area infested in 2002 (fig. 1), and The natural enemies predominantly Progeny of interspecific (i.e., interspecies) 17 infestations found outside this area to used against the sharpshooter are tiny crosses and backcrosses to V. vinifera were date have been eradicated. The success of mymarid wasps in the genus Gonatocerus, evaluated for a spectrum of horticultural the GWSS control program shows it can which lay their eggs inside the eggs of and quality traits in addition to resis- be a model for responding to other pest the sharpshooter. Approximately 2.4 mil- tance to X. fastidiosa (Viana et al. 2011). invasions. However, the potential remains lion of these wasps have been released Aggressive vine training, which forced for GWSS populations to flare up, as in California to date (CDFA 2013). These flowering of 2-year-old seedlings, and ap- evidenced by increased trap counts, and efforts have involved a collaborative re- plication of DNA marker technology gen- spread to new areas or resistance to cur- sponse from CDFA (Larry Bezark, David erated progeny of the fourth backcross, rent control methods could develop, re- Morgan, Charlie Pickett), UC Riverside expected to be genetically 97% V. vinifera, quiring that program measures continue (Ali Al-Wahibi, Mark Hoddle, Nick Irvin, in only 10 years. Test-size lots of wine and prompting recent initiation of studies Rodrigo Krugner, Joseph Morse, Leigh have been made from grapes of previous on resistance management. Pilkington, Serguei Triapitsyn) and USDA generations and currently are being made While insecticide treatments have (Greg Simmons). from fourth backcross generation selec- proven critical to keeping GWSS popula- tions. Release of PD-resistant varieties Genetic approaches to combating PD tions low and preventing the spread and with a range of wine styles is anticipated establishment of GWSS in new areas of Genetic resistance is generally re- (Walker and Tenscher 2012). The breeding California, biological control is also used garded as the most reliable control program continues. as part of an integrated management ap- measure for a readily transmitted plant Efforts in other laboratories have trans- proach. Biological control efforts began in disease. Although there is apparent varia- ferred specific genes from nongrapevine the late 1990s, when explorations for natu- tion in the susceptibility of European sources, referred to as transgenes, into V. ral enemies were conducted in the native grapevine (V. vinifera) varieties to X. vinifera. The advantage of the transgenic range of GWSS (Triapitsyn et al. 1998). fastidiosa, all succumb to PD (Hopkins approach is that it greatly increases the The Temecula PD outbreak stimulated and Purcell 2002). The research group of number of sources of resistance beyond additional searches for biological control Andrew Walker at UC Davis discovered what is available in conventional breed- agents, and testing, rearing, release and both apparently single-gene and multiple- ing. Ten years ago, only a few sketchy monitoring of natural enemies are now gene resistance in other Vitis species notions were available on how to create

2002 2014

Butte

Sacramento

Madera Santa Clara Santa Clara Fresno Fresno Tulare Tulare

Kern Kern Santa San Bernardino Santa San Bernardino Barbara Ventura Los Barbara Ventura Los Angeles Angeles

Orange Riverside Orange Riverside

San Imperial San Imperial Diego Diego GWSS-infested area

Fig. 1. Areas of California infested by GWSS in 2002 and 2014. At the end of 2002, GWSS was confined mostly to Southern California counties, with minor infestations in three Northern California counties. The Southern California infestation in 2014 is slightly expanded compared to the infestation in 2002, but some Northern California infestations have been eradicated. Other infestation maps are available at cdfa.ca.gov/pdcp/map_index.html.

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 137 transgenes capable of interfering with use could be grafted onto the transgenic clever experimental approaches for devel- X. fastidiosa infection of grapevine or the rootstock line and be at least partially oping transgenic resistance to X. fastidiosa mechanisms on which they might oper- protected against X. fastidiosa. in grapevines. ate. Infecting X. fastidiosa bacterial cells The transformed lines that have been Fusion of two proteins. One straightfor- reside not in the living cells of the plant, examined closely are indistinguishable ward approach to reducing the titer of where a transgene product normally from the untransformed lines from which X. fastidiosa in grapevine xylem is to would accumulate, but in the xylem, the they were derived (Dandekar et al. 2011; discover or develop a protein capable array of dead cells that form the vascular Lindow et al. 2014), suggesting that the of killing or preventing the increase of elements responsible for conducting water vines have the quality and horticultural X. fastidiosa cells and then to deliver that and minerals from the roots into the aer- traits of the untransformed lines. This protein to the xylem. A research group ial parts of the plant. Responding to this result is expected because the transfor- headed by Abhaya Dandekar at UC Davis challenge, researchers not only identified mation process introduces only a minute and including Goutam Gupta of Los various genetic elements that encode change in the plant genome. In commer- Alamos National Laboratory conceived molecules that restrain the accumulation cialization, combinations of several trans- the approach of fusing two proteins, each and/or spread of X. fastidiosa but also ele- genes acting through distinct biochemical with some activity against X. fastidiosa, ments that deliver these molecules to the mechanisms of action likely would be into a single, xylem-targeted protein. xylem. Importantly, several of the mol- introduced into a grapevine line to obtain One protein of the fusion pair binds to a ecules were shown to cross graft unions at least additive resistance effects and to specific protein that is abundant on the and to confer, as a transgenic rootstock, greatly reduce the chance that a variant surface of the X. fastidiosa cell. The other protection to a grafted nontransgenic X. fastidiosa would be able to overcome re- protein breaches the X. fastidiosa cell scion. Rootstock-conferred resistance has sistance. The following paragraphs sum- membrane, thereby killing the bacterial obvious versatility: Varietal scions now in marize five mechanistically diverse and cell. Both proteins killed X. fastidiosa cells

Coordinated response to PD involves growers, scientists and government he academic and government research on GWSS and PD 1996 Treceived support from the state’s viticulture and enology UC ANR forms Viticulture Consortium (VC), funded by a grant industries and even local government before and during the from USDA Cooperative State Research, Education, and Extension Temecula Valley outbreak. Industry organizations partner- Service (USDA CSREES, now USDA NIFA, National Institute of Food ing with CDFA and UC Division of Agriculture and Natural and Agriculture). Resources (UC ANR) in these efforts included the American Report of GWSS establishment in Southern California Vineyard Foundation, the California Table Grape Commis- is published. sion, the California Raisin Board and the California Rootstock Commission. UC ANR and CDFA provided 1997 coordination to prioritize research, Industry-matched state funds initiate the California Competitive avoid duplication and maximize Grant Program for Research in Viticulture and Enology (CCGPRVE). the collective benefits of the programs. Since 1999, USDA 1998 has provided about 75% of Search for biological control agents for GWSS begins. the funding for PD control 1999 and research, and the state of California, industry and Temecula Valley vineyards show severe damage from PD; GWSS is UC have provided the recognized as the vector. rest. California legislation Riverside County declares emergency; the county and city of initiated a statewide as- Temecula each contribute $125,000 for research. sessment on wine grapes UC appoints Pierce’s Disease Research and Emergency Response to support research and Task Force to identify strategies for combating PD. related activities, raising CDFA appoints task force with members from UC, California State about $46 million to date University, CDFA, county agricultural commissioners, USDA and (Tumber et al. 2014; Wig- industry to identify PD/GWSS research priorities. gins 2001). The timeline here Jack Kelly Clark Jack Kelly highlights some of the key CA Assembly Bill 1232 provides $2.25 million over 3 years to be events in the efforts to contain matched by $0.75 million in industry funds for PD/GWSS research; and find solutions to the PD out- the CDFA competitive grants program is funded. break in California.

138 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 in culture, but the fusion protein was sig- protein to be secreted into the xylem, in the plant, whereas spread of mutants nificantly more potent than either protein where infecting X. fastidiosa cells colonize that overproduce XfDSF is severely re- component alone. Grapevines expressing the vine. Greenhouse-grown plants were stricted (Chatterjee et al. 2008). the fusion protein showed significant pro- found to have reduced disease symptoms Transfer of a gene whose product cata- tection against PD (Dandekar, Gouran et compared to unaltered grapevines when lyzes XfDSF synthesis should result in ac- al. 2012). inoculated with a high dose of X. fastidiosa cumulation of XfDSF even in the absence HxfA protein. Bruce Kirkpatrick’s (Kirkpatrick et al. 2012). of X. fastidiosa and, after inoculation with laboratory at UC Davis identified a pro- XfDSF, pathogen confusion. Steven X. fastidiosa, should constrain movement tein of X. fastidiosa, HxfA, which, when Lindow and his research associates at UC and accumulation of X. fastidiosa and re- inactivated, surprisingly led to increased Berkeley intensely investigated intercel- duce PD symptom extent and intensity. virulence of the bacterium (Guilhabert lular communication of X. fastidiosa and These expected results have been ob- and Kirkpatrick 2005). This result sug- applied their findings to suppress the served (Lindow et al. 2012, 2014). gests that, when active, HxfA suppresses spread of the bacterium in the plant using Programmed cell death. The char- virulence. Perhaps a grapevine line that a phenomenon they refer to as pathogen acteristic scorching symptoms of PD produces HxfA could reduce PD severity confusion. X. fastidiosa secretes a specific were shown by the laboratory of David by decreasing the virulence of infecting 14-carbon fatty acid and possibly other Gilchrist at UC Davis to be an example X. fastidiosa, and infecting X. fastidiosa similar molecules as diffusible signal fac- of the phenomenon known as genetically would be less successful at inducing PD tors (XfDSF). As X. fastidiosa populations programmed cell death, where the symp- than in unaltered vines. Grapevine plants grow, the concentration of XfDSF around toms resulted from a reaction of the plant producing full-length or truncated ver- the cells increases. Compared to the unal- to the presence of a bacterium (X. fastidi- sions of HxfA were constructed. The tered bacterium, X. fastidiosa mutants that osa) rather than directly to an action of genes were designed to cause the HxfA fail to produce XfDSF spread more readily that bacterium (Gilchrist et al. 2007). This

2000 2004 UC is awarded USDA CSREES grant of $2 million to establish a CDFA and UC competitive PD/GWSS research programs combine competitive grants program for PD/GWSS research; annual fund- their proposal review processes. ing was renewed eight times. CDFA-requested report “California Agricultural Research Priorities: UC establishes Pierce’s Disease Competitive Grants Program. Pierce’s Disease” is published by National Research Council of the CA Senate Bill 671 provides funds for a coordinated statewide ef- National Academies. fort against PD/GWSS. Number of GWSS biological control agents released in California Federal government declares emergency and provides $22.3 mil- since 1999 exceeds 1 million. lion for GWSS containment and PD research. 2005 First GWSS infestation is found outside the generally infested California wine grape growers vote to continue statewide PD/ Southern California area, in Contra Costa County; eradication ef- GWSS wine grape assessment. forts begin. 2008 CDFA adopts emergency regulations to prevent spread of GWSS on shipments of nursery stock, bulk grapes and (later) citrus. Nursery Stock Approved Treatment Protocol established to re- duce need for GWSS inspections. 2001 2010 CA Assembly Bill 1394 creates the Pierce’s Disease and Glassy- Winged Sharpshooter Board and an assessment on wine grapes California wine grape growers vote again to continue statewide to fund PD/GWSS research and related activities; this assessment PD/GWSS wine grape assessment, with option to support re- raised $46 million through February 2014. search and outreach on other wine grape pests and diseases. First area-wide management program begins in Kern County, 2011 testing methods for controlling PD and GWSS in large and diverse Last CCGPRVE-supported project completed, and the agricultural areas. program ends. First annual PD/GWSS research symposium takes place. 2013 2002 Last projects funded by USDA-UC and VC are completed; these GWSS infestation found in Contra Costa County in 2000 is de- programs end. clared eradicated, marking the first successful eradication of a Industry-funded CDFA competitive grants program continues, localized GWSS infestation. with its proposal review process now conducted under UC ANR’s Unified Grant Management for Viticulture and Enology. c

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 139 Varietal scions now in use could be grafted onto the transgenic rootstock line and be at least partially protected against X. fastidiosa.

protection against X. intractable in molecular terms. Over the fastidiosa. Protection years, research projects were supported at and level of PGIP 16 universities and at several government accumulation were laboratories, and the continued funding positively correlated from various sources, including grower- in different trans- voted assessments (see sidebar, pages formed grapevine 138–9), resulted in numerous advances in lines (Aguero et al. our understanding of the biology of the 2005). PGIP is natu- disease and the development of effective rally targeted to the control measures. xylem, and PGIP- The entire genome sequence of Gregory Urquiaga generating rootstocks X. fastidiosa became available, and pro- UC Davis plant scientist Abhaya Dandekar and colleagues have fused protected grafted cedures for creating mutants of the two genes to engineer resistance to Pierce’s disease of grapevines. nontransgenic scions. bacterium and introducing new genes The untransformed were developed and applied (Guilhabert research group searched a large collection scion was demonstrated to accumulate et al. 2001; Guilhabert and Kirkpatrick of grapevine genes for the ability of spe- PGIP from its PGIP-transgenic rootstock, 2003; Newman et al. 2004; Van Sluys et cific nucleotide sequences to confer pro- suggesting that transported PGIP is the al. 2003). Genetic variation in X. fastidiosa tection against programmed cell death in actual agent of protection in the scion was characterized as to its origins and tomato roots. Two of these grapevine nu- (Dandekar, Gilchrist et al. 2012; Labavitch its determination of host range (Nunney cleotide sequences, when transferred back et al. 2012). 2011; Nunney et al. 2013). Individual into grapevine, suppressed PD symptoms Tests of transformed grapevine lines events in the association of X. fastidiosa and prevented death of the X. fastidiosa- were performed first in the greenhouse, with the sharpshooter and the establish- inoculated plants (Harvey et al. 2008). and outdoor trials of these newly devel- ment of feeding sites by the sharpshooter Moreover, the bacterial titer was reduced oped grapevine materials were begun in have been revealed (Almeida and Purcell by 4 to 6 orders of magnitude relative to March 2010. The field trials are expected 2003; Almeida et al. 2005; Son et al. 2012). the titer in untransformed control vines, to yield valuable information on the feasi- The arrays of grapevine messenger RNAs which died in 2 to 3 months. In the trans- bility of developing these approaches into (responsible for directing the synthesis formed plants, X. fastidiosa titers were re- commercial applications (Gilchrist et al. of proteins) that accumulate under vari- duced to a level that should result in only 2012; Miller et al. 2012). ous situations were characterized and rare or no acquisition by the sharpshooter. revealed grapevine genes that specifi- Research advances One of the nucleotide sequences, when in- cally respond to X. fastidiosa infection but troduced into the rootstock only, was able The seriousness of the GWSS-borne not to drought (Choi et al. 2010, 2013). In to protect untransformed scions (Gilchrist X. fastidiosa threat to the California wine cold curing, X. fastidiosa was found to and Lincoln 2009). and grape industries was realized early be cleared not by the effects of low tem- PG-inhibiting protein (PGIP). The in the Temecula Valley PD outbreak, and peratures alone but by the grapevine’s X. fastidiosa genome has one gene for effective cooperation between federal, response to the cold (Feil and Purcell the enzyme polygalacturonase (PG), an state and county agricultural agencies, in- 2001; Lieth et al. 2011). Obviously, these enzyme that cleaves homogalacturonan, dustry groups, and UC followed. Actions research advances would not have been a major component of the intercellular taken to combat the Temecula Valley PD possible without the sources of research matrix that joins the walls of adjacent epidemic and prevent its spread were rap- support indicated above. The new discov- plant cells. A X. fastidiosa strain with an idly mounted, and funding from federal, eries have elevated the bacterium, the in- inactive PG was unable to move long dis- state and industry sources has supported sect vector and the plant host close to the tance in the inoculated plant or to induce both control measures and basic and ap- level of a model research system and cre- PD symptoms (Roper et al. 2007). UC plied research. A summary of current ated a foundation for new management Davis researchers Abhaya Dandekar, John research and control costs associated with strategies in the future. c Labavitch and Ann Powell lead research PD appeared recently (Tumber et al. 2014), groups that have demonstrated interfer- and the sidebar below indicates some of ence with X. fastidiosa accumulation in the research expenditures. plants by the action of a PG-inhibiting Of the biological actors in the epidemic G. Bruening, B.C. Kirkpatrick and R.K. Webster are all Professor Emeritus, Department of Plant Pathology, protein (PGIP). The PGIP from pear fruit (X. fastidiosa, GWSS and grapevine), UC Davis; T. Esser is Special Assistant, Pierce’s Disease was found to be effective in inhibiting none was regarded in 1999 as being Control Program, California Department of Food and bacterial PG. The pear PGIP gene was well characterized in research terms, Agriculture, Sacramento. moved into grapevine, where it provided and all seemed at the time to be almost

140 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 References Aguero CB, Uratsu SL, Greve C, et al. 2005. Evaluation Feil H, Feil WS, Purcell AH. 2003. Effects of date of Miller T, Daugherty M, Mauk P. 2012. Field trial for resis- of tolerance to Pierce’s disease and Botrytis in trans- inoculation on the within-plant movement of Xylella tance to Pierce’s disease. In: Esser T (ed.). Pierce’s Disease genic plants of Vitis vinifera L. expressing the pear PGIP fastidiosa and persistence of Pierce’s disease within field Research Progress Reports. CDFA, Sacramento. p 175–7. gene. Mol Plant Pathol 6(1):43–51. doi:10.1111/j.1364- grapevines. Phytopathology 93(2):244–51. doi:10.1094/ www.cdfa.ca.gov/pdcp/research.html. 3703.2004.00262.x. phyto.2003.93.2.244. Newman KL, Almeida RPP, Purcell AH, et al. 2004. Cell-cell Almeida RPP, Purcell AH. 2003. Transmission of Xylella Feil H, Purcell AH. 2001. Temperature-dependent growth signaling controls Xylella fastidiosa interactions with both fastidiosa to grapevines by Homalodisca coagulata and survival of Xylella fastidiosa in vitro and in pot- insects and plants. P Natl Acad Sci USA 101(6):1737–42. (Hemiptera:Cicadellidae). J Econ Entomol 96(2):264–71. ted grapevines. Plant Dis 85(12):1230–4. doi:10.1094/ Nunney L. 2011. Homologous recombination and the in- doi:10.1603/0022-0493-96.2.264. pdis.2001.85.12.1230. vasion of a new plant host by the pathogenic bacterium, Almeida RPP, Wistrom C, Hill BL, et al. 2005. Vector trans- Gilchrist DG, Lincoln JE. 2009. Systemic control of Pierce’s Xylella fastidiosa. Phytopathology 101(6):S130. mission of Xylella fastidiosa to dormant grape. Plant Dis disease by altered expression of anti-apoptotic genes Nunney L, Vickerman DB, Bromley RE, et al. 2013. Recent 89(4):419–24. doi:10.1094/pd-89-0419. or their RNA-based regulatory elements. In: Esser T (ed.). evolutionary radiation and host plant specialization in Anas O, Harrison UJ, Brannen PM, et al. 2008. The effect of Pierce’s Disease Research Symposium. CDFA, Sacramento. the Xylella fastidiosa subspecies native to the United warming winter temperature on the severity of Pierce’s p 10–11. www.cdfa.ca.gov/pdcp/research.html. States. Appl Environ Microb 79(7):2189–200. doi:10.1128/ disease in the Appalachian mountains and Piedmont Gilchrist DG, Lincoln JE, Cook DR. 2007. Resistance to aem.03208-12. of the southeastern United States. Plant Health Prog- Pierce’s disease by transgenic expression of plant-derived Purcell A, Finley AH. 1979. Evidence for noncirculative ress. www.plantmanagementnetworkorg/pub/php/ anti-apoptotic genes. In: Esser T (ed.). Pierce’s Disease Re- transmission of Pierce’s disease bacterium by sharp- research/2008/pierces. doi:101094/PHP-2008-0718-01-RS. search Symposium. CDFA, Sacramento, CA. p 252–5. shooter leafhoppers. Phytopathology 69:393–5. Andersen PC, Brodbeck BV, Mizell RF. 2003. Plant and Gilchrist D, Lincoln J, Kominek T, et al. 2012. Field evalua- Purcell AH, Saunders SR. 1999. Fate of Pierce’s disease insect characteristics in response to increasing density tion of grape plants expressing potential protective DNA strains of Xylella fastidiosa in common riparian plants in of Homalodisca coagulata on three host species: A sequences effective against Pierce’s disease. In: Esser T California. Plant Dis 83(9):825–30. quantification of assimilate extraction. Entomologia (ed.). Pierce’s Disease Research Progress Reports. CDFA, Redak R, Bethke J. 2003. Toward a standardized treatment Experimentalis Et Applicata 107(1):57–68. doi:10.1046/ Sacramento. p 109–11. www.cdfa.ca.gov/pdcp/research. protocol to eliminate glassy-winged sharpshooter egg j.1570-7458.2003.00036.x. html. masses in commercial nursery stock. In: Esser T (ed.). [CDFA] California Department of Food and Agriculture. Grafton-Cardwell EE, Reagan CA, Ouyang Y. 2003. Insecti- Pierce’s Disease Research Symposium. CDFA, Sacramento. 2001. Pierce’s Disease Control Program, Report to the cide treatments disinfest nursery citrus of glassy-winged p 308–10. Legislature, January 1, 2001 (2000 Report). www.cdfa. sharpshooter. Calif Agri 57(4):128–31. Redak RA, Purcell AH, Lopes JRS, et al. 2004. The biol- ca.gov/pdcp/ReportsToLegislature.html. 33 p plus ap- Guilhabert MR, Hoffman LM, Mills DA, et al. 2001. Trans- ogy of xylem fluid-feeding insect vectors of Xylella pendices. poson mutagenesis of Xylella fastidiosa by electropora- fastidiosa and their relation to disease epidemiology. CDFA. 2005. Pierce’s Disease Control Program, Report tion of Tn5 synaptic complexes. Mol Plant Microbe In Annu Rev Entomol 49:243–70. doi:10.1146/annurev. to the Legislature, April 2005 (2004 Report). www.cdfa. 14(6):701–6. ento.49.061802.123403. ca.gov/pdcp/ReportsToLegislature.html. 28 p plus ap- Guilhabert MR, Kirkpatrick BC. 2003. Transformation of Roper MC, Greve LC, Warren JG, et al. 2007. Xylella fastidi- pendices. Xylella fastidiosa with broad host range RSF1010 deriva- osa requires polygalacturonase for colonization and CDFA. 2013. Pierce’s Disease Control Program, Report to tive plasmids. Mol Plant Pathol 4(4):279–85. doi:10.1046/ pathogenicity in Vitis vinifera grapevines. Mol Plant Mi- the Legislature (2012 Report). www.cdfa.ca.gov/pdcp/ j.1364-3703.2003.00175.x. crobe In 20(4):411–9. doi:10.1094/mpmi-20-4-0411. ReportsToLegislature.html, www.cdfa.ca.gov/pdcp/ Guilhabert MR, Kirkpatrick BC. 2005. Identification of Son Y, Backus EA, Groves RL, et al. 2012. Pattern of stylet map_index.html. 24 p. Xylella fastidiosa antivirulence genes: Hemagglutinin ad- penetration activity by Homalodisca vitripennis (Hemip- Chatterjee S, Wistrom C, Lindow SE. 2008. A cell-cell hesins contribute to X. fastidiosa biofilm maturation and tera: Cicadellidae) adults in relation to environmental signaling sensor is required for virulence and insect colonization and attenuate virulence. Mol Plant Microbe temperature and light conditions. Environ Entomol transmission of Xylella fastidiosa. P Natl Acad Sci USA In 18(8):856–68. 41(5):1215–30. doi:10.1603/en11319. 105:2670–5. Harvey JJW, Lincoln JE, Gilchrist DG. 2008. Programmed Triapitsyn SV, Mizell RF, Bossart JL, et al. 1998. Egg parasit- Choi HK, da Silva FG, Lim HJ, et al. 2010. Diagnosis of cell death suppression in transformed plant tissue oids of Homalodisca coagulata (Homoptera: Cicadellidae). Pierce’s disease using biomarkers specific to Xylella fastidi- by tomato cDNAs identified from an Agrobacterium Fla Entomol 81:241–3. osa rRNA and Vitis vinifera gene expression. Phytopathol- rhizogenes-based functional screen. Mol Genet Genomics Tumber KP, Alston JM, Fuller KB. 2014. Pierce’s disease ogy 100(10):1089–99. doi:10.1094/phyto-01-10-0014. 279(5):509–21. doi:10.1007/s00438-008-0329-2. costs California $104 million per year. Calif Agr 68(1– Choi HK, Iandolino A, da Silva FG, et al. 2013. Water deficit Hopkins DL, Purcell AH. 2002. Xylella fastidiosa: Cause 2):20–9. modulates the response of Vitis vinifera to the Pierce’s of Pierce’s disease of grapevine and other emergent Van Sluys MA, de Oliveira MC, Monteiro-Vitorello CB, et al. disease pathogen Xylella fastidiosa. Mol Plant Microbe In diseases. Plant Dis 86(10):1056–66. doi:10.1094/ 2003. Comparative analyses of the complete genome se- 26(6):643–57. doi:10.1094/mpmi-09-12-0217-r. pdis.2002.86.10.1056. quences of Pierce’s disease and citrus variegated chloro- Dandekar AM, Gilchrist D, Miller T, et al. 2012. Chimeric Kabashima J, Gutman G, Redak R, et al. 2011. GWSS Nurs- sis strains of Xylella fastidiosa. J Bacteriol 185(3):1018–26. antimicrobial protein and polygalacturonase-inhibiting ery Approved Treatment Best Management Practices. doi:10.1128/jb.185.3.1018-1026.2003. protein transgenic grapevine field trial. In: Esser T (ed.). CDFA. 23 p. Varela LG, Smith RJ, Phillips PA, et al. 2001. Pierce’s Dis- Pierce’s Disease Research Progress Reports. Sacramento: Kirkpatrick BC, Lincoln JE, Roper C, et al. 2012. Evaluation ease. UC ANR Pub 21600. Oakland, CA. p 20. California Department of Food and Agriculture. p 94–103. of Pierce’s disease resistance in transgenic Vitis vinifera Viana AP, Riaz S, Walker MA. 2011. Evaluating genetic www.cdfa.ca.gov/pdcp/research.html. grapevines expressing either grape thaumatin-like pro- diversity and optimizing parental selections in a seg- Dandekar AM, Gilchrist D, Miller T, et al. 2011. Chimeric tein or Xylella fastidiosa hemagglutinin protein. In: Esser T regating table-grape population. Am J Enol Viticult antimicrobial protein and polygalacturonase-inhibiting (ed.). Pierce’s Disease Research Symposium. CDFA, Sacra- 62(3):285–90. doi:10.5344/ajev.2011.10073. protein transgenic grapevines field trial. In: Esser T (ed.). mento. p 130–6. Walker A, Riaz S. 2012. Genetic mapping of Xylella Pierce’s Disease Research Progress Reports. Sacramento: Labavitch JM, Powell ALT, Bennett A, et al. 2012. Optimiz- fastidiosa resistance gene(s) in grape germplasm from California Department of Food and Agriculture. p 101–6. ing grape rootstock production and export of inhibitors southern United States. In: Esser T (ed.). Pierce’s Disease www.cdfa.ca.gov/pdcp/research.html. of Xylella fastidiosa polygalacturonase activity. In: Esser T Research Symposium. CDFA, Sacramento. p 241–7. Dandekar AM, Gouran H, Ibanez AM, et al. 2012. An en- (ed.). Pierce’s Disease Research Symposium. CDFA, Sacra- gineered innate immune defense protects grapevines mento. p 147–53. Walker A, Tenscher A. 2012. Breeding to Pierce’s disease resistant winegrapes. In: Esser T (ed.). Pierce’s Disease Re- from Pierce disease. P Natl Acad Sci USA 109(10):3721–5. Lieth JH, Meyer MM, Yeo K-H, et al. 2011. Modeling cold search Symposium. CDFA, Sacramento. p 233–40. doi:10.1073/pnas.1116027109. curing of Pierce’s disease in Vitis vinifera ‘Pinot Noir’ and Daugherty MP, Almeida RPP. 2009. Estimating Xylella ‘Cabernet Sauvignon’ grapevines in California. Phytopa- Weare BC. 2009. How will changes in global climate influ- fastidiosa transmission parameters: Decoupling sharp- thology 101:1492–500. ence California? Calif Agri 63(2):59–66. shooter number and feeding period. Entomologia Lindow SE, Ionescu M, Baccari C, et al. 2012. Enhancing Webster RK, Nation SP. 2000. Report of the University of Experimentalis Et Applicata 132(1):84–92. doi:10.1111/ control of Pierce’s disease by augmenting pathogen sig- California Pierce’s Disease Research and Emergency Re- j.1570-7458.2009.00868.x. nal molecules. In: Esser T (ed.). Pierce’s Disease Research sponse Task Force. UC Office of the President. 62 p. Davis MJ, Purcell AH, Thomson SV. 1978. Pierce’s disease Progress Reports. CDFA, Sacramento. p 154–66. www. Wiggins P. 2001. Food and Agriculture Code, Amend. Cali- of grapevines — isolation of causal bacterium. Science cdfa.ca.gov/pdcp/research.html. fornia State Assembly Bill 1394. Pests: Pierce’s disease and 199(4324):75–7. doi:10.1126/science.199.4324.75. Lindow S, Newman K, Chatterjee S, et al. 2014. Produc- the Glassy-winged Sharpshooter. http://www.leginfo. tion of Xylella fastidiosa diffusible signal factor in trans- ca.gov/pub/01-02/bill/asm/ab_1351-1400/ab_1394_ genic grape causes pathogen confusion and reduction bill_20010725_chaptered.html. in severity of Pierce’s disease. Mol Plant Microbe In 27(3):244–54. doi:10.1094/mpmi-07-13-0197-fi.

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 141 MAINTAINING LONG-TERM MANAGEMENT nce pests and diseases become established, their interactions with crops, landscapes or animals are in a continuous Ostate of flux, depending on environmental conditions and changes in pest control practices. Their long-term management is never static; it relies on a combination of techniques and strategies. The articles in this section take the long view and present how UC scientists tackle the evolution of a pest problem — herbicide resistance — and how the UC Statewide IPM program has managed pests while minimizing environmental risks for 35 years.

Herbicide-resistant weeds challenge some signature cropping systems

by Bradley D. Hanson, Steven Wright, Lynn M. Sosnoskie, Albert J. Fischer, Marie Jasieniuk, John A. Roncoroni, Kurt J. Hembree, Steve Orloff, Anil Shrestha and Kassim Al-Khatib

Invasive and endemic weeds pose recurring challenges for California land managers. ndemic and invasive weeds are The evolution of herbicide resistance in several species has imposed new challenges important management concerns in California due to their direct in some cropping systems, and these issues are being addressed by UC Cooperative E and indirect costs to agriculture, the Extension farm advisors, specialists and faculty. There are currently 24 unique environment and society. Pimentel et al. herbicide-resistant weed biotypes in the state, dominated by grasses and sedges in (2005) estimated that weeds cost U.S. crop flooded rice systems and, more recently, glyphosate-resistant broadleaf and grass producers and pasture managers over $30 billion in control-related expenses and weeds in tree and vine systems, roadsides and glyphosate-tolerant field crops. Weed reduced productivity. Although specific scientists address these complex issues using approaches ranging from basic physiol- data are not available for California’s ogy and genetics research to applied research and extension efforts in grower fields portion of these losses, weed manage- throughout the state. Although solutions to herbicide resistance are not simple and are ment costs for the state’s 40 million acres of crop and grazing lands, as well as the affected by many biological, economic, regulatory and social factors, California stake- remaining 60 million acres of land area, holders need information, training and solutions to address new weed management amount, undoubtedly, to several billion problems as they arise. Coordinated efforts conducted under the Endemic and Invasive dollars annually. In addition to the direct Pests and Disease Strategic Initiative directly address weed management challenges in cost of weed control and lost agricultural productivity, weeds also affect ecosystem California’s agricultural industries. quality and function, reduce recreational access and degrade aesthetics in natu- ral areas, change wildland fire regimes and severity, and impede water flow through rivers and canals, among other Anil Shrestha Anil negative impacts. Although crop weeds are seldom considered as being “invasive” in the traditional sense, novel biotypes can develop, spread and subsequently oc- cupy a greater proportion of crop acreage than might normally be expected. For example, when a weed population evolves resistance to an herbicide or any other control measure, a “routine” pest can become a new and serious problem. The first case of an herbicide-resistant weed in California was reported in 1981 by UC scientists (Holt et al. 1981); in recent years, additional species have evolved resistance to various herbicide chemistries (table

Online: http://californiaagriculture.ucanr.edu/ A stone fruit orchard in Fresno County is dominated by glyphosate-resistant horseweed. Reliance on one method of weed control imposes selection pressure, which can lead to population shifts to tolerant landingpage.cfm?article=ca.v068n04p142&fulltext=yes species or selection of resistant biotypes. doi: 10.3733/ca.v068n04p142

142 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 1) used in some of California’s signature in a community dominated by different of a species to become resistant to cropping systems, including flooded rice, species adapted to the new conditions an herbicide. Herbicide resistance orchards and vineyards as well as nearby (Hanson et al. 2013). This weed shift can arises from the process of adaptive noncrop areas. be caused by agronomic and horticultural evolution, whereby mutations change the practices (tillage, fertility, irrigation, etc.) physiology of plants in such a way that How do weeds become resistant to or by the use of herbicides, which are very the herbicide is less effective. Under the herbicides? strong selective agents. Some species will continued selection pressure exerted by Environmental factors and production be less susceptible (more tolerant) than the herbicide(s), resistant plants with the practices influence species composition others to any management practice, and new genotype are not controlled, and at any location, a phenomenon known as repeated use of the same control strategy their offspring build up in the popula- selection pressure. Under constant condi- can shift weed populations to become tion (fig. 1B). Depending on the initial tions, the weed community will become dominated by naturally tolerant species frequency and genetic basis of resistance, dominated by species that thrive under (fig. 1A). the regularity and rate of herbicide ap- those conditions. If this steady state is Herbicide resistance, on the other plications, and the reproductive system of upset by a change in management prac- hand, implies that a genetic change has the weed, it may take from a few to many tices, a weed shift may occur, resulting caused a formerly susceptible population generations for resistance to become

TABLE 1. Important herbicide modes of action

Mode of action WSSA group Target site and effects Herbicide examples ACCase inhibitors 1 Several important classes include aryloxyfenoxypropionates, Clethodim, cyhalofop, diclofop, cyclohexanediones and phenylpyrazolin. These herbicides inhibit the fluazifop, pinoxaden, sethoxydim, many enzyme acetyl coenzyme A carboxylase (ACCase), which leads to the others disruption of lipid synthesis at the growing point of susceptible grasses.

ALS inhibitors 2 Several herbicide classes including the imidazolinones and sulfonylureas Bensulfuron, chlorsulfuron, and others inhibit the enzyme acetolactate synthase (ALS), which halosulfuron, imazamox, imazethapyr, disrupts synthesis of branched-chain amino acids. metsulfuron, rimsulfuron, sulfometuron, many others

Carotenoid synthesis 11, 12, 13, 27 Several unrelated chemical classes block enzymes important in the Amitrole, clomazone, fluridone, inhibitors synthesis of carotenoids and/or chlorophyll. Because carotenoids protect mesotrione, norflurazon, topramezone, plants from excess oxidative energy, lack of carotenoids usually results in others membrane and protein damage from free radicals.

Cellulose inhibitors 20, 21, 27 Several chemical classes inhibit aspects of cell wall (cellulose) synthesis. Dichlobenil, indaziflam, isoxaben, quinclorac

EPSPS inhibitors 9 The glycine herbicides inhibit the enzyme 5-enolypyruvylshikimate-3- Glyphosate phosphate synthetase (EPSPS), which is important in the synthesis of aromatic amino acids.

Fatty acid and lipid synthesis 8, 16, 26 Several chemical classes, including the thiocarbamates, inhibit processes Bensulide, butylate, EPTC, molinate, inhibitors important in the synthesis of fatty acid and lipids, impacting production triallate, vernolate, others of membranes, proteins, hormones and other cellular components.

Glutamine synthetase 10 Phosphonic acid herbicides inhibit the enzyme glutamine synthetase. Glufosinate inhibitors Blocking of this process leads to buildup of ammonia in the plant and also inhibits PSII and PSI.

Mitosis inhibitors 3, 15, 23 Several different chemical families affect various processes important in Alachlor, dimethenamid, metolachlor, cell division. The most widely used include chloroacetemides (Group 3) oryzalin, pendimethalin, pronamide, and dinitroaniline (Group 15) herbicides. trifluralin, many others

Photosystem I inhibitors (PSI) 22 PSI inhibitors divert electrons during photosynthesis and create free Paraquat, diquat radicals that quickly degrade cell membranes and lead to cell and tissue desiccation.

Photosystem II inhibitors (PSII) 5, 6, 7 Herbicide classes including the triazines, uracils, amides and several Atrazine, bromacil, diuron, hexazinone, others disrupt photosynthesis by blocking electron transport in PSII. linuron, propanil, simazine, Plant death usually occurs from protein and lipid oxidation caused by tebuthiuron, others free radicals.

Synthetic auxins 4 Benzoic acids, phenoxycarboxylic acids, pyrachlor and pyridine 2,4-D, aminocyclopyrachlor, carboxylic acids mimic endogenous auxins. At high concentrations, aminopyralid, clopyralid, dicamba, these growth regulator herbicides lead to uncontrolled cell division and MCPA, quinclorac, triclopyr, others growth and can stimulate ethylene production.

For a more complete listing and description of herbicide modes of action, refer to the Weed Science Society of America (WSSA) website at http://wssa.net/wp-content/uploads/ WSSA-Mechanism-of-Action.pdf.

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 143 apparent (Jasieniuk et al. 1996; Maxwell et 1957, herbicide-resistant weed biotypes commonly occurring among weedy spe- al. 1990). have been reported in at least 60 coun- cies. However, in recent years, glyphosate tries and include more than 400 unique (glycine herbicide) resistance and multiple Current status of herbicide resistance species-herbicide group combinations resistances (resistance to two or more her- The strongest selection pressure for (fig. 2A). The United States has more bicides with dissimilar modes of action) herbicide-resistant weeds tends to be in herbicide-resistant biotypes (162) than have also emerged as major problems in modern, high-intensity agricultural crop- any other country (fig. 2B), and California some cropping systems. Interestingly, ping systems due to a high reliance on accounts for 21 of these (fig. 2C, table 2). while herbicide resistance in the United herbicides. According to the International Worldwide, resistance to acetolactate States as a whole is primarily found in Survey of Herbicide Resistant Weeds synthase (ALS)–inhibiting herbicides broadleaf weeds, California has more (weedscience.org), since the first con- and photosystem II (PSII)–inhibiting her- herbicide-resistant grasses or sedges (15) firmed report of a resistant biotype in bicides (Groups 5, 6 and 7) are the most than broadleaf species (6) (table 2). Due to the extensive use of preplant and in-season tillage in some agronomic crops in California, along with the use of pre- and postemergence herbicides,

Bradley D. Hanson D. Bradley herbicide resistance is not as widespread as it is in other parts of the country where no-till and minimum-till systems have been widely adopted. Reduced tillage systems are heavily reliant on a few her- bicide modes of action (e.g., glyphosate) and have correspondingly larger prob- lems with herbicide resistance (Culpepper 2006). In contrast to the rest of the United States, where herbicide resistance prob- lems are centered on agronomic crops, the greatest problems with herbicide- resistant weeds in California are in or- chards, vineyards, flooded rice, roadsides Glyphosate-resistant horseweed in a raisin vineyard near Parlier, left, and glyphosate-resistant ryegrass and irrigation canal banks. Herbicide- in a walnut orchard near Davis. resistant weeds have become especially

A. Species shift

B. Resistance

Initial population Population after years of selection pressure

Fig. 1. Herbicides impose selection pressure and can lead to weed species shifts, resulting in populations dominated by more-tolerant species (A). Occasionally, an individual weed has a mutation that confers resistance to an herbicide or group of herbicides, and this individual survives and reproduces despite being treated with herbicide (B). In both cases, after several generations and repeated selection with the same or similar herbicides, the tolerant species or resistant biotype can become dominant in the population. (Modified from Orloff et al. 2009 with permission.)

144 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 450 challenging problems in California’s signature cropping sys- A. Reported HRW worldwide tems, which are characterized by little or no crop rotation due 400 to soil limitations (rice) or long cropping cycles (orchards and Glycine 350 vineyards) and relatively few opportunities for mechanical ALS inhibitor weed control. Although large by specialty crop standards, the Other approximately 3 million acres devoted to orchard, vineyard 300 ACCase inhibitor and rice production in California is a small market for herbicide Bipyridilium 250 Multiple-resistant manufacturers; thus, herbicide options are somewhat limited. Dinitroanaline Combined, these factors have led to a high degree of selection 200 PSII inhibitor pressure for herbicide-resistant weed biotypes as well as weed Synthetic auxin population shifts to naturally tolerant species (Hanson et al. 150 2013; Prather et al. 2000). No. unique HRW species 100

TABLE 2. Confirmed cases of herbicide-resistant weeds in California 50

Scientific name Common name Year Mode of action* 0 Senecio vulgaris Common groundsel 1981 PSII inhibitor 1970 1975 1980 1985 1990 1995 2000 2005 2010 Lolium perenne Perennial ryegrass 1989 ALS inhibitor 175 Cyperus difformis Smallflower umbrella 1993 ALS inhibitor B. Reported HRW in the United States sedge 150 Sagittaria California arrowhead 1993 ALS inhibitor montevidensis Salsola tragus Russian-thistle 1994 ALS inhibitor 125 Avena fatua Wild oat 1996 Pyrazolium (difenzoquat) 100 Ammannia auriculata Eared redstem 1997 ALS inhibitor

Schoenoplectus Ricefield bulrush 1997 ALS inhibitor 75 mucronatus Echinochloa Late watergrass 1998 Thiocarbamate phyllopogon No. unique HRW species 50 Echinochloa Late watergrass 1998 Multiple (ACCase phyllopogon inhibitor, ALS inhibitor, 25 thiocarbamate and clomazone) Lolium rigidum Rigid ryegrass 1998 Glycine 0 1970 1975 1980 1985 1990 1995 2000 2005 2010 Ammannia coccinea Redstem 2000 ALS inhibitor 25 Echinochloa crus-galli Barnyardgrass 2000 Multiple (ACCase inhibitor and C. Reported HRW in California thiocarbamate)

Echinochloa Late watergrass 2000 Thiocarbamate 20 phyllopogon Echinochloa oryzoides Early watergrass 2000 Multiple (ACCase inhibitor and thiocarbamate) 15 Phalaris minor Small-seeded 2001 ACCase inhibitor canarygrass

Digitaria ischaemum Smooth crabgrass 2002 Synthetic auxin 10 Conyza canadensis Horseweed 2005 Glycine No. unique HRW species Lolium perenne ssp. Italian ryegrass 2005 Glycine multiflorum 5 Conyza bonariensis Hairy fleabane 2007 Glycine Echinochloa colona Junglerice 2008 Glycine Conyza bonariensis Hairy fleabane 2009 Multiple (glycine and 0 bipyridylium) 1970 1975 1980 1985 1990 1995 2000 2005 2010 Year Cyperus difformis Smallflower umbrella 2013 PSII sedge Fig. 2. Chronological increase in reports of herbicide-resistant weeds Poa annua Annual bluegrass 2013 Glycine (HRW) worldwide and in the United States and California. Data compiled in August 2013 from the International Survey of Herbicide Resistant Weeds * PSII = photosystem II, ALS = acetolactate synthase, ACCase = acetyl coenzyme A carboxylase. (weedscience.org).

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 145 UC weed scientists address herbicide etc.), researchers often conduct field or goal of these efforts is to help growers and resistance in weeds greenhouse tests to verify and quantify pest control advisers recognize the im- the level of resistance. Plants from the portance of taking a proactive approach In order to combat complex issues suspected herbicide-resistant population to preventing the evolution of a resistant such as herbicide resistance, organized are treated with the herbicide of interest population, rather than a reactive ap- collaborations between weed scientists at rates ranging from below normal doses proach to managing herbicide resistance and other agricultural researchers with a to doses well above those legally allowed after it occurs. wide array of expertise are required. This in the field (see photos, below). The re- Target-site resistance occurs when includes the activities of UC Cooperative sponse (i.e., plant growth or mortality) of the enzyme that is the target of the her- Extension farm advisors and special- the putative resistant population is then bicide becomes less sensitive, or fully ists, Agricultural Experiment Station compared with the response of the known insensitive, to the herbicide, often due to faculty, support scientists, research staff susceptible, or wild-type, population. a physical change in the target enzyme’s and graduate students, as well as faculty Resistance is confirmed if the herbicide af- structure. These physical changes can from other universities and agricultural fects the two (or more) populations of the impair the ability of the herbicide (or industry representatives (for a list of UC same species in markedly different ways other herbicides) to attach to a specific weed scientists, visit the Weed Research with respect to plant growth and survival. binding site on the enzyme, thus reduc- and Information Center at wric.ucdavis. In many cases, an estimate of the level of ing or eliminating herbicidal activity. edu). Current herbicide-resistant weed resistance also is made from these data. Target-site resistance is sometimes evalu- management efforts range from applied For example, if the susceptible popula- ated at the tissue level using portions of research and extension efforts to basic tion is controlled at one-half the field rate, plants such as leaves, leaf disks or roots plant biology and evolutionary ecology but the resistant population survives at (see photos, next page). In some cases, a studies. Although the specifics vary, twice the field rate, it would be described functioning target enzyme (e.g., ALS or these efforts can be grouped into three as having a fourfold (2 / 0.5 = 4) level acetyl coenzyme A carboxylase [ACCase]) general areas: (1) applied management of resistance. can be extracted and its function evalu- of herbicide-resistant plants, (2) physiol- Physiology and mechanisms of herbi- ated in laboratory in vitro experiments in ogy and mechanisms of resistance and cide resistance. Identifying and verifying the presence or absence of the herbicide. (3) biology, ecology and evolution of herbicide resistance and developing alter- Recently, overproduction or enhanced herbicide resistance. native management strategies provides activity of the target enzyme has been Applied management of herbicide- short-term solutions for weed managers. shown to confer herbicide resistance in resistant plants. Many cases of herbicide Researchers often conduct further studies certain cases (Gaines et al. 2011). resistance in weeds are identified after to determine the underlying molecular Several mechanisms of nontarget-site growers, land managers or pest control and physiological causes of resistance and resistance confer resistance to herbicides advisers observe weed control failures to compare the biology, growth and com- in plants without involving the target with treatments that were once effec- petitive ability of herbicide-resistant spe- sites of the herbicides. This can result tive. These weeds are generally brought cies and biotypes. The mechanism(s) and in unpredictable resistance to unrelated to the attention of local or statewide fitness costs of herbicide resistance can herbicides (Délye 2013; Délye et al 2013). Cooperative Extension personnel. If the have important ramifications on the selec- Of these, the best-known cases involve herbicide application method is ruled out tion, spread and competitive ability of resistance in which herbicide-resistant as the cause of poor weed control (i.e., herbicide-resistant biotypes, in addition to plants have an enhanced ability to meta- incorrect product, rate, timing, placement, directly impacting their management. The bolically degrade the herbicide to less- or Marcelo Moretti Marcelo Moretti Marcelo

Glyphosate-susceptible population Glyphosate-resistant population

Orchard-collected junglerice plants 21 days after treatment in a greenhouse dose-response experiment. The pot at the farthest left in each photo was untreated, and the remaining plants were treated with glyphosate rates ranging from (left to right) 1⁄32×, 1⁄16×, 1⁄8×, ¼×, ½×, 1×, 2× and 4× of the labeled use rate. The glyphosate-susceptible population was controlled with a ¼ use rate, while the resistant population had some survivors at the 4× rate.

146 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 nontoxic forms. Many processes can be involved in metabolic resistance, but the most well-understood cases are due to changes in three groups of isozymes (cy- tochrome P450 monoxidases, glutathione transferases and glycosyltransferases) and changes in ATP-binding cassette (ABC) transporters (Yuan et al. 2007). This type of resistance is most commonly evaluated using nonherbicidal inhibitors of the vari- ous isozymes in the presence or absence of the herbicide and comparing metabolic degradation of the herbicide in laboratory or greenhouse assays. Biology, ecology and evolution of her- bicide resistance. Many factors influence Hanson D. Bradley the evolution of herbicide resistance in weed populations (reviewed in Jasieniuk et al. 1996). To design effective resistance management strategies for the long term, UC and other scientists are conducting basic research on weed biology and on ecological and evolutionary processes in weed populations. In a few cases, the mechanisms that confer resistance to herbicides have al- tered the fitness (i.e., survival, growth Hanson D. Bradley Hanson D. Bradley and/or seed production) of resistant In some cases of herbicide-resistant weeds, enzyme- or tissue-level assays can be used to understand plants, as compared with susceptible and quantify resistance. Above, a lab assistant collects leaves from suspected glyphosate-resistant plants of the same species in the absence horseweed; left, leaf disks from the intact leaves are cut for an in vivo assay; right, disks are incubated overnight in the laboratory in buffer solutions containing various concentrations of glyphosate in order of herbicide treatment. Differential plant to evaluate activity of the EPSPS enzyme. fitness among biotypes can affect the rate at which herbicide resistance can spread. can help inform growers of emerging her- glyphosate. This herbicide is, by far, the For example, if resistant and susceptible bicide-resistant weed populations while most widely used herbicide in the state plants have equal fitness, the number of they are still localized; surveys are also in perennial crop production systems, as resistant plants in the population would often used to encourage adoption of re- well as in many roadsides, canal banks not change relative to the number of sus- sistance mitigation measures to minimize and residential and industrial areas. ceptible plants during periods when the economic and environmental impacts. Glyphosate-tolerant (Roundup Ready) cot- herbicide was not being applied (Jasieniuk Further, surveys combined with popula- ton, alfalfa and corn are becoming widely et al. 1996). In contrast, if resistant plants tion genetic research can determine the adopted in the state, which will further are less fit than susceptible plants, the evolutionary and geographic origins, and increase selection pressure for additional number of resistant plants may decrease routes of spread, of resistance across an glyphosate-resistant and -tolerant species. during periods when herbicide is not agricultural landscape (e.g., Okada et al. Herbicide resistance in flooded rice. applied. Fitness is usually evaluated by 2013; Okada et al. 2014). Most California rice is produced in mono- growing resistant and susceptible plants culture systems due to impeded soil Herbicide resistance in California in direct competition with one another, or drainage, which limits rotation to other with the crop of interest, and comparing Herbicide resistance has been an upland crops (Hill et al. 2006). Rice fields relative productivity or fecundity. important management concern in are kept under continuous flood condi- Similar to efforts for other invasive California flooded rice production for sev- tions during the growing season, primar- weeds, insects and disease pathogens, eral years (Busi et al. 2006). Weeds with ily for the control of grass weeds (Strand surveys are sometimes used to delineate resistance to the ALS inhibitors (Group 2), 2013). Although this system favors sedges the extent of population growth or the thiocarbamates (Group 8) and ACCase in- and other water-tolerant weeds, selective expansion of new herbicide-resistant hibitors (Group 1) are the dominant weed herbicides such as molinate and bensul- weed biotypes. Because there often are a management problems in most of the furon provided highly effective weed few escaped weeds in herbicide-treated Sacramento Valley rice production region. control for several years. However, in the fields, herbicide resistance may not be In orchards and vineyards, herbicide early 1990s, after repeated use, resistance recognized until the resistant biotype resistance is a more recent development to the ALS-inhibiting herbicide bensul- makes up a significant portion of the local and is dominated by resistance to the furon became widespread among weedy population (Vencill et al. 2012). Surveys broad-spectrum postemergence herbicide species in rice. By 2000, several additional

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 147 weed biotypes with resistance to ALS with multiple resistance to propanil Herbicide resistance in orchard and inhibitors, thiocarbamates or ACCase and bensulfuron were identified in the vineyard cropping systems. The first her- inhibitors had evolved and were causing Sacramento Valley (Abdallah et al. 2014). bicide-resistant weed in orchard cropping significant weed management, economic Late watergrass (Echinochloa phyllo- systems was perennial ryegrass, Lolium and environmental issues in the rice crop- pogon) populations resistant to ACCase perenne (now named Festuca perennis spp. ping system. UC researchers, extension inhibitors, ALS inhibitors and the thio- perenne), reported in 1989 (Heap 2013). personnel and industry partners have de- carbamate herbicides in rice systems were This ALS inhibitor–resistant biotype was voted considerable efforts to understand- reported in 1998 (Fischer, Ateh et al. 2000; selected on roadsides by the use of sul- ing and managing herbicide-resistant Fischer, Bayer et al. 2000). This resistance fometuron and, thus far, has not been a weeds in rice. to multiple herbicides within an individ- major problem in orchards or vineyards Smallflower umbrella sedge (Cyperus ual plant indicated that using herbicides because relatively little of this class of her- difformis) and California arrowhead with different modes of action would be bicides is used in these crops. However, (Sagittaria montevidensis) resistance to unlikely to provide satisfactory control of several ALS inhibitors, including rim- ALS-inhibiting herbicides was first re- the species in the long term. Further com- sulfuron, penoxsulam, halosulfuron and ported in California rice fields in 1993 plicating the situation in rice, populations flazasulfuron, are becoming more widely following repeated use of bensulfuron of late watergrass and barnyardgrass used in tree and vine crops, and selection (Hill et al. 1994). Field research has shown (Echinochloa crus-galli) with resistance pressure for ALS inhibitor resistance may that California arrowhead is a fairly weak to both ACCase inhibitors and thiocar- increase in the future. competitor in rice systems (Gibson et al. bamates, and thus exhibiting multiple The first case of glyphosate resistance 2001) and that the ALS-resistant biotypes resistance, were reported in 2000. Later in California was reported in a popula- can be adequately controlled with other research confirmed that the mechanisms tion of rigid ryegrass (Lolium rigidum, registered herbicides. Recently, small- of multiple resistance to several herbicide now Festuca perennis spp. rigidium) in flower umbrella sedge biotypes with classes are due to metabolic degradation 1998 (Simarmata and Penner 2008). multiple resistance to the PSII herbicide of these compounds (Yasuor et al. 2008, However, most confirmed glyphosate- propanil and to several ALS-inhibiting 2009). resistant ryegrass populations have been herbicides were identified in the Smooth crabgrass (Digitaria isch- identified as Italian ryegrass (Lolium Sacramento Valley (Valverde et al. 2014), aemum) resistance to the synthetic auxin multiflorum, now Festuca perennis spp. mul- and research is ongoing to elucidate the herbicide quinclorac was reported in 2002. tiflorum) (Sherwood and Jasieniuk 2009). mechanisms of resistance and any cross Detailed research into the mechanisms Glyphosate-resistant ryegrasses have resistance to other rice herbicides. of resistance suggested that the cause become widespread and are a major weed Eared redstem (Ammannia auriculata) was an altered sensitivity in the auxin problem in orchards, vineyards and road- and ricefield bulrush (Schoenoplectus response pathway, leading to ACCase sides of Northern California (Jasieniuk mucronatus) resistance to ALS inhibitor activity, ethylene synthesis and enhanced et al. 2008). Research indicated that resis- herbicides in rice was reported in 1997. ability to detoxify cyanide (a byproduct tance in ryegrass is not due to metabo- Redstem research has focused on intra- of ethylene biosynthesis) (Abdallah et al. lism of the herbicide and is instead due and interspecific competition in an effort 2006). Although crabgrass is not an im- to an altered EPSPS enzyme (Jasieniuk to develop agronomic solutions to reduce portant rice weed, quinclorac is used in et al. 2008; Simarmata and Penner 2008). its competition with rice (Caton et al. 1997; rice systems for control of other weeds, Glyphosate resistance in these areas Gibson et al. 2003). Studies have shown and resistance to it has been reported in has been largely driven by decreases in that California populations of ricefield Echinochloa species of rice in California grower use of other herbicides, especially bulrush are resistant to most registered (Yasuor et al. 2011) and from other re- those under increasing regulatory pres- ALS inhibitors, whereas populations gions. Most importantly, the observed sure because of pesticide contamination from other regions are resistant only to changes in ethylene synthesis and pro- of ground or surface water. The use of one chemical family, the sulfonylureas, duction of toxic byproducts may also re- glyphosate-based herbicide programs also in the ALS inhibitor group (Busi et al. late to the plant’s ability to tolerate abiotic increased when the patent on Roundup 2006). Recently, ricefield stress. Two implications of this finding expired in 2000 and low-cost, generic bulrush biotypes include the possibilities that (1) quinclo- glyphosate herbicides became readily rac-resistant smooth crabgrass has the po- available. Today, glyphosate accounts for tential to invade a more diverse range of over 60% of all herbicide-treated acreage habitats and become an important weed in California orchard and vineyard sys- of rice; and (2) adaptation to the abiotic tems (DPR 2013). stress of the flooded environments Glyphosate-resistant horseweed, or may predispose Echinochloa phyllo- mare’s tail (Conyza canadensis), was re- pogon or other major rice weeds to ported in 2005 and is one of the dominant evolve resistance to quinclorac in weeds in and around raisin and tree the future. fruit production areas of the San Joaquin Valley, as well as on roadsides and canal banks in the region (Hanson et al. 2009; Barnyardgrass (Echinochloa crus-galli). Hembree and Shrestha 2007; Shrestha,

148 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 Joseph DiTomaso Importance of herbicide resistance in weeds of natural areas by Joseph M. DiTomaso

orldwide, the majority of the plant species that are develop- weed control option, such as mechanical or cultural control prac- Wing herbicide resistance are those that occur as weeds in tices. For a number of reasons, including economic feasibility and agricultural environments, on roadsides and in other rights-of-way. the potential for damage to desirable (nontarget) vegetation, it is In contrast, herbicide resistance is not nearly so common in weeds uncommon for a land manager to reapply the same herbicide for of natural areas or rangelands. A search of the International Survey several consecutive years in a natural area. of Herbicide Resistant Weeds (weedscience.com) revealed no her- Because the evolution of herbicide resistance is typically the bicide-resistant weeds (i.e., invasive nonnative species) listed for ter- result of intensive, persistent selective pressure on a rapidly regen- restrial natural areas anywhere in the world, and only two resistant erating weed population (i.e., annual species), the incidence of weeds listed for aquatic areas, both of them in Florida. In pastures, herbicide-resistant species would be expected to be much higher 15 species worldwide have developed resistance, eight of which are in a cropping system with limited rotations or in other systems, considered primarily as agricultural weeds. Only two of those 15 are found in pastures within the United States, and none occurs in any Western state. The reason more weeds develop herbicide resistance in agri- cultural and right-of-way systems has to do with factors associated with characteristics of specific weeds, herbicides and weed man- agement practices. For example, high seed production increases the opportunity for genetic variation, and with it the probability that a resistance adaptation will occur. It so happens that all of the major weeds that have developed resistance to herbicides are annuals. In an agricultural system, annual species make up the vast majority of problematic weeds. Annuals can have high seed Joseph DiTomaso Joseph DiTomaso production, rapid turnover of the seedbank (due to a high percent- Yellow starthistle (Centaurea solstitialis) infestation, left; aerial spraying age of seed germination each year) and, in some cases, several to control yellow starthistle near Sierra Foothill Research and Extension reproductive generations per growing season. This increases the Center, right. selective pressure for herbicide-resistant biotypes. In natural areas such as rights-of-way, that are continuously managed with herbi- of California, the California Invasive Plant Council (Cal-IPC) lists 214 cides. In many natural areas, the effort to manage invasive plants flowering plants as invasive cal-ipc.org( ). Of these, only 27.5% are can involve several different control strategies besides, or instead of, annual species; the remainder (and the majority) are either woody herbicide application. These can include mechanical means such species or herbaceous perennials or biennials. Perennial weeds, and as mowing, cultural methods including grazing management or particularly those with vegetative reproductive tissues, are less likely prescribed burning and, when available, biological control agents. than annuals to evolve herbicide resistance. Furthermore, even when herbicides are used, they are rarely applied The choice of herbicide can also increase or decrease the likeli- repeatedly over a long period of time. The total area of noncropped hood that weeds will develop herbicide resistance. In most natural lands treated with herbicides is far smaller than the total acreage areas, herbicides are not used as intensively as in croplands, where of agricultural land treated with herbicides. It is hardly surprising, it is common to repeat herbicide applications within a single year then, that the incidence of herbicide resistance in natural areas or over several consecutive years. In addition, fewer herbicides are and rangelands is low — in fact, it is not even reported at present available for use in natural areas of California, and the most widely in California. used compounds (e.g., 2,4-D, aminopyralid, dicamba, triclopyr Regardless of the vegetative environment, whether natural or or clopyralid) belong to the growth regulator chemical families. agricultural, prevention of herbicide resistance and management Resistance to these herbicides does not develop as commonly as of established resistant weed populations could be accomplished resistance to other herbicide families, despite their having more effectively if we put a greater reliance on integrated been available and extensively used for a long time. weed management approaches. Although the likelihood that Glyphosate is also commonly used in natural areas, resistance will develop in natural areas is already low, man- and although glyphosate resistance is on the rise in agement strategies that employ rotation of herbicides cropping systems, its development is often associ- with different modes of action, the use of competitive ated with repeated applications over multiple years, a species in restoration programs, and a combination strategy not generally used in natural areas. of mechanical, biological and cultural control options Weed management practices are often in an integrated management program will further reduce the most important contributing factors leading to the the selective pressure on invasive plant populations and with selection of herbicide-resistant biotypes. In general, a it the potential that weeds will develop herbicide resistance. land manager’s complete and repeated reliance on a single herbicide or mode of action for weed control can greatly enhance the occurrence of herbicide-resistant weeds. This J.M. DiTomaso is UC Cooperative Extension Specialist, Department of Plant Sciences, is particularly true when the manager uses no other UC Davis.

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 149

Jack Kelly Clark Hembree, Wright 2008; Shrestha et al. Hembree 2008). Glyphosate resistance in confer resistance to these dissimilar herbi- 2010). The level of glyphosate resistance hairy fleabane appears to be similar to cides, and research is ongoing to elucidate in horseweed is relatively low, and resis- resistance in horseweed in that (1) selec- these factors. tant plants are usually injured to some tion has occurred in response to similar Junglerice (Echinochloa colona) resistant degree following glyphosate applications, management strategies in perennial crops to glyphosate was first identified in 2008 which suggests that resistance is not due and surrounding areas (Hembree and in a Roundup Ready corn field in the to an altered target enzyme. Genetic com- Shrestha 2007); (2) multiple origins of re- Sacramento Valley (Alarcon-Reverte et parisons of horseweed accessions from sistance are suspected (Okada et el. 2014); al. 2013); since then, glyphosate-resistant around the state suggest that there have and (3) growth stage and environmental junglerice has become widespread in been multiple, independent origins of conditions affect the level of resistance orchards and field crops throughout resistance in this species, rather than the (Moretti, Hanson et al. 2013; Shrestha California (Moretti, Garcia et al. 2013). spread of resistance from a single-source et al. 2007). The discovery by Moretti, Resistance appears to be due to mutations population (Okada et al. 2013). Hanson et al. (2013) of hairy fleabane re- in the EPSPS target site (Alarcon-Reverte Hairy fleabane (Conyza bonariensis) sistant to both glyphosate and paraquat et al. 2013), although some populations populations resistant to glyphosate were raises questions about whether a common also appear to have enhanced EPSPS reported in 2007 (Shrestha, Hanson, physiological mechanism is helping to activity (A.J. Fischer, unpublished data).

Herbicide-resistant weeds unlikely in vegetable crops by Steve Fennimore, Richard Smith and Michelle Le Strange

eed management systems in California vegetable crops can and improved tolerance to herbicides. Mechanical cultivation is Wbe described as robust, complex, multitactic and integrated. facilitated with smooth seedbeds and good tilth, which allows the Vegetable herbicides generally make up just one component in cultivation equipment to remove weeds that are close to the crop a multicomponent weed management system. With California’s row. Increasingly, growers are using precision guidance systems to seasonally dry weather and growers’ ability to control soil moisture improve the speed and accuracy of cultivation. by means of irrigation scheduling, it becomes possible for the Preirrigation and use of a stale seedbed. Preirrigation before grower to apply effective cultural and physical control practices, final seedbed preparation is a common practice, as it stimulates a such as preparation of stale seedbeds and inter-row cultivation. weed flush a few days after watering. As soon as the weeds have Redundancy is designed into the weed management system to emerged and the field is dry enough to enter, the grower uses shal- minimize weed emergence in the crop. The key tools that make low cultivation, flaming or a nonselective herbicide to remove the up an integrated vegetable weed management system are field new weeds. Research has shown this technique to provide 15% to selection, sanitation, crop rotation, land preparation, stale seedbeds, 50% control of weeds in crops like lettuce (Shem Tov et al. 2006). herbicides and physical weed control (UC IPM 2009). Growers who The combination of stale seedbed technique and both herbicides carefully apply these practices are able to manage weeds effectively and cultivation often results in good weed control. and reduce the presence of weed seeds in the soil seedbank. Herbicides. One category of herbicide used in vegetable crops Field selection. Farmers often grow vegetable crops on fields is fumigants, such as metam potassium, which is applied 14 to 21 that have low weed pressure so their weed control operations can days before planting to kill weed seeds and germinating seedlings. be more efficient and economical. They use translocated herbicides After planting, soil-active herbicides like pronamide (used in arti- during fallow periods to control troublesome perennial weeds like chokes and head lettuce) and S-metolachlor and trifluralin (used field bindweed. in tomatoes and peppers) are applied to provide preemergence Sanitation. Growers often keep vegetable fields and the sur- control of weeds. Postemergence herbicides are utilized in some rounding areas as weed-free as possible to keep the weeds from crops; examples include clethodim, used to control emerged grass going to seed. Some operations that utilize a “zero weed seed” weeds in many broadleaf vegetable crops, and oxyfluorfen and philosophy have successfully reduced weed pressure in subsequent bromoxynil, used to control broadleaf weeds. Many vegetable her- vegetable crops by eliminating weed seed inputs to the soil seed- bicides were developed in the 1960s and 1970s and include prod- bank. Other measures such as cleaning all field equipment when ucts like DCPA (used in broccoli and onion), napropamide (used in moving it from a weedy field or into a clean field are also employed. tomatoes and peppers) and linuron (used in asparagus and celery). Rotation. By growing vegetable crops in rotation with crops Given the complexity of the vegetable weed control program and that normally have more intensive weed control programs, growers the extensive use of cultivation and hand-weeding, the selective can help keep a field clean of weeds. Because field conditions are pressure on weeds from vegetable herbicides is very light, despite constantly changing under a rotation system, no one weed species their decades of use. is likely to become dominant. Physical weed control. Vegetable growers make extensive use Land preparation. Direct-seeded vegetable crops require well- of physical weed control. One example is inter-row cultivation or prepared seedbeds free of large clods to facilitate precision planting shallow cultivation between the crop rows to control weeds. Inter- and allow rapid and uniform emergence of vegetable seedlings. row cultivation is a very old but effective method that buries, cuts A uniform seeding depth is critical to uniform crop emergence or uproots weeds. Hand-weeding by workers with hoes is the last

150 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 Target-site mutations appear to be the been initiated to verify and characterize using various postemergence and pre- most frequent mechanism among the the putative resistant populations. emergence herbicides along with mechan- accessions so far collected in California; ical control measures in an integrated California herbicide resistance research: however, additional research is ongoing to approach. Applied research integrating Locally applied research and exten- determine whether the same is true with agronomy, weed control, spray applica- sion with national and international populations selected in orchards and in tion technology and water management implications other regions of the Central Valley. have been useful to regulatory agencies Several other common weeds in or- Since the discovery of herbicide- (e.g., California Department of Pesticide chards and vineyards, including Palmer resistant weed biotypes in California, Regulation and California Environmental amaranth (Amaranthus palmeri), three- UC research and Cooperative Extension Protection Agency) and have had positive spike goosegrass (Eleusine tristachya) personnel, as well as university and non- impacts on water and air quality, wildlife and witchgrass (Panicum capillare), are university cooperators and students, have habitat and water use (Pittelkow et al. suspected to have evolved resistance to conducted locally relevant weed manage- 2012). glyphosate; preliminary research trials ment research in the state. Research and Information on the underlying mecha- by UC researchers and California State extension efforts have included alterna- nisms and genetic basis of resistance University, Fresno, collaborators have tive chemical management techniques provides useful information to California

line of defense against weeds in vegetable crops. Among the hoe- populations. Adding to the cost for growers who practice “zero ing crew, manual dexterity and good depth perception allow the weed seed tolerance” is the physical removal of troublesome weeds workers to carefully remove weeds from the vegetable crop in the such as flowering nightshades and dodder to prevent seeding and row and near the crop plant. Hand-weeding is expensive and can further field contamination. The harvest operation undercuts all cost $300 or more per acre in organic vegetable plantings and high- plants growing on the bed top, and after harvest the field is quickly density plantings (e.g., spinach and baby lettuces) — sometimes a tilled under, killing any remaining weeds before the field is rotated lot more. to another crop. Integrated weed management in lettuce. In a typical lettuce The lettuce and tomato weed management systems are inten- weed control program, the crop is grown on a field with a light sive and redundant, made up of many operations conducted in weed population, so one tool growers use is field selection. Some- sequence with the aim of minimizing weed emergence. In practice, times the soil is fumigated with metam potassium before planting these weed management systems are not always as flawless as the to control weeds and soilborne diseases, but most lettuce is grown above descriptions might suggest. Crops like broccoli and cauli- on nonfumigated land. Prior to planting, the soil is irrigated to flower are grown during winter months, when extended rain and stimulate weed emergence and then shallow-tilled to kill weeds and wet field conditions prevent cultivation and hand-weeding. Other form a smooth seedbed for planting. At time of seeding, preemer- complications are high-density plantings such as those used for gence herbicides such as pronamide or bensulide are applied, to spinach, which limit the grower’s ability to cultivate. be activated with the initial sprinkler irrigation. About 4 weeks after Overall, the chances are low that weeds will develop herbicide emergence, the lettuce is hand-thinned and weeded by a hoeing resistance in a vegetable crop planting. Technology is evolv- crew to its final stand. Inter-row cultivation in furrows and on bed ing that will allow intelligent robotic cultivators to tops is conducted one or more times, also removing weeds. Finally, remove weeds from the intra-row space without about 6 weeks after lettuce emergence, the field is hand-weeded the use of herbicides, so there is reason for opti- to remove any remaining weeds. After harvest, the field is quickly mism that the development of herbicide-re- tilled under, killing any remaining weeds before the field is rotated sistant weeds in California vegetable fields to another crop. will remain low for the foreseeable future. Integrated weed management in tomatoes. Virtually all Cali-

fornia tomatoes are transplanted, and 75% are grown using subsur- Clark Jack Kelly face drip irrigation buried 8 to 10 inches deep. Fields with low weed populations, especially those free of field bindweed and dodder, S. Fennimore is UC Cooperative Extension (UCCE) are most often sought for tomato production. Beds are preirrigated Specialist, Department of Plant Sciences, UC Davis; R. Smith is UCCE Farm Advisor, Monterey County; to germinate weeds, then cultivated and shaped prior to planting. and M. Le Strange is UCCE Farm Advisor Emeritus, Typically only two herbicide applications are made: one just prior Tulare County. to planting or at planting, and the other at layby. Herbicides such as halosulfuron, pendimethalin, rimsulfuron, S-metolachlor, sulfen- trazone and trifluralin are used, depending upon the site and weed spectrum. Just prior to layby application, beds and furrows are me- References Shem-Tov S, Fennimore SA, Lanini WT. 2006. Weed management in lettuce chanically cultivated. (Lactuca sativa) with pre-plant irrigation. Weed Technol 20:1058–65. These practices significantly reduce weed emergence and com- UC IPM. 2009. Integrated weed management. In: Spinach: UC IPM Pest Manage- petition against the young tomato crop. Hoeing crews may hand- ment Guidelines. UC ANR Pub 3467. Oakland, CA. www.ipm.ucdavis.edu/PMG/ weed once or twice before or after layby, depending on weed r732700111.html.

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 151 weed managers in the longer term. This herbicide resistance are not simple and information is broadly applicable to the are affected by many biological, economic, biology, physiology, evolution and con- regulatory and social factors. The diverse B.D. Hanson is UC Cooperative Extension (UCCE) trol of weeds in other crops and regions network of weed scientists and collabora- Specialist, Department of Plant Sciences, UC Davis; at the local, national and international tors in a land-grant university system is S. Wright is UCCE Farm Advisor, Tulare County; L.M. Sosnoskie is Project Scientist, Department of Plant level. Although this paper has focused well positioned to address these complex Sciences, UC Davis; A.J. Fischer is Professor, Department on the efforts of UC weed scientists and issues and respond to stakeholder con- of Plant Sciences, UC Davis; M. Jasieniuk is Professor, collaborators, the basic and applied scien- cerns through applied and basic research, Department of Plant Sciences, UC Davis; J.A. Roncoroni tific information developed in California extension and outreach to affected agri- is UCCE Farm Advisor, Napa County; K.J. Hembree is supports similar research being con- cultural industries, and education of fu- UCCE Farm Advisor, Fresno County; S. Orloff is UCCE ducted in other regions of the country ture scientists and leaders. Ultimately, the Farm Advisor and County Director, Siskiyou County; A. Shrestha is Professor, Department of Plant Science, and world. goal of weed science research is to help California State University, Fresno; K. Al-Khatib is Like many other areas encompassed growers maintain agricultural productiv- Director, UC Statewide Integrated Pest Management by the Endemic and Invasive Pests and ity and economic stability while increas- Program. Diseases Strategic Initiative, solutions to ing environmental sustainability. c

References Abdallah I, Fischer AJ, Elmore CL, et al. 2006. Mechanism Heap I. 2013. The International Survey of Herbicide Re- Pittelkow CM, Fischer AJ, Moechnig MJ, et al. 2012. of resistance to quinclorac in smooth crabgrass (Digitaria sistant Weeds. www.weedscience.com (accessed August Agronomic productivity and nitrogen requirements of ischaemum). Pestic Biochem Physiol 84:38–48. 30, 2013). alternative tillage and crop establishment systems for Abdallah IS, Garcia A, Fischer AJ. 2014. Rice field bulrush Hembree K, Shrestha A. 2007. Control of glyphosate- improved weed control in direct-seeded rice. Field Crop (Schoenoplectus mucronatus (L.) Palla) evolved multiple resistant marestail and hairy fleabane in orchards and Res 130:128–37. resistances to propanil and bensulfuron herbicides. J Biol vineyards. California Weed Science Society Proc 59:113–7. Prather TS, DiTomaso JM, Holt JS. 2000. Herbicide resis- Chem Res 31:788–99. Hill JE, Smith RJ, Bayer DE. 1994. Rice weed control: Cur- tance: Definitions and management strategies. UC ANR Alarcon-Reverte R, Garcia A, Urzua J, Fisher AJ. 2013. Re- rent technology and emerging issues in temperate rice. Pub 8012. Oakland, CA. 12 p. sistance to glyphosate in junglerice (Echinochloa colona) Aust J Exp Agr 34:1020–9. Sherwood AM, Jasieniuk M. 2009. Molecular identifica- from California. Weed Sci 61:48–54. Hill JE, Williams JF, Mutters RG, Greer CA. 2006. The tion of weedy glyphosate-resistant Lolium (Poaceae) in Busi R, Vidotto F, Fischer AJ, et al. 2006. Patterns of resis- California rice cropping system: Agronomic and natural California. Weed Res 49:354–64. tance to ALS herbicides in smallflower umbrella sedge resource issues for long-term sustainability. Paddy Water Shrestha A, Hanson BD, Fidelibus MW, Alcorta M. 2010. (Cyperus difformis) and ricefield bulrush (Schoenoplectus Environ 4:13–9. Growth, phenology, and intraspecific competition be- mucronatus). Weed Technol 20:1004–14. Holt JS, Stemler AJ, Radosevich SR. 1981. Differential tween glyphosate-resistant and glyphosate-susceptible Caton BP, Foin TC, Hill JE. 1997. Mechanisms of competi- light responses of photosynthesis by triazine-resistant horseweeds (Conyza canadensis) in the San Joaquin Val- tion for light between rice (Oryza sativa) and redstem and triazine-susceptible Senecio vulgaris biotypes. Plant ley of California. Weed Sci 58:147–53. (Ammannia spp.). Weed Sci 45:269–75. Physiol 67:744–8. Shrestha A, Hanson BD, Hembree KJ. 2008. Glyphosate- [DPR] California Department of Pesticide Regulation. Jasieniuk M, Ahmad R, Sherwood AM, et al. 2008. resistant hairy fleabane documented in the Central Val- 2013. Pesticide use reporting. www.cdpr.ca.gov/docs/ Glyphosate-resistant Italian ryegrass (Lolium multiflorum) ley. Calif Agr 62:116–9. pur/pur11rep/11_pur.htm (accessed on March 1, 2013). in California: Distribution, response to glyphosate, and Shrestha A, Hembree KJ, Va N. 2007. Growth stage influ- Culpepper SA. 2006. Glyphosate-induced weed shifts. molecular evidence for an altered target enzyme. Weed ences level of resistance in glyphosate-resistant horse- Weed Technol 20:277–81. Sci 56:496–502. weed. Calif Agr 61:67–70. Délye C. 2013. Unraveling the genetics bases of non- Jasieniuk M, Brule-Babel AL, Morrison IN. 1996. The evolu- Shrestha A, Hembree K, Wright S. 2008. Biology and man- target-site-based resistance (NTSR) to herbicides: A major tion and genetics of herbicide resistance in weeds. Weed agement of horseweed and hairy fleabane in California. challenge for weed science in the forthcoming decade. Sci 44:176–93. UC ANR Pub 8314. Oakland, CA. p 9. Pest Manag Sci 69:176–87. Maxwell BD, Roush ML, Radosevich SR. 1990. Predicting Simarmata M, Penner D. 2008. The basis for glyphosate Délye C, Jasieniuk M, Le Corre V. 2013. Deciphering the the evolution and dynamics of herbicide resistance in resistance in rigid ryegrass (Lolium rigidum) from Califor- evolution of herbicide resistance in weeds. Trends Genet weed populations. Weed Technol 4:2–13. nia. Weed Sci 56:181–8. 29:649–58. Moretti ML, Garcia AM, Fischer AJ, Hanson BD. 2013. Dis- Strand L. 2013. Integrated Pest Management for Rice (3rd Fischer AJ, Ateh CM, Bayer DE, Hill JE. 2000. Herbicide- tribution of glyphosate-resistant junglerice (Echinochloa ed.). UC ANR Pub 3280. Oakland, CA. 98 p. resistant Echinochloa oryzoides and E. phyllopogon in Cali- colona) in perennial crops of the Central Valley of Califor- Valverde BE, Boddy LG, Pedroso RM, et al. 2014. Cype- fornia Oryza sativa fields. Weed Sci 48:225–30. nia. Proc Western Soc Weed Sci 66:19. rus difformis evolves resistance to propanil. Crop Prot Fischer AJ, Bayer DE, Carriere MD, et al. 2000. Mecha- Moretti ML, Hanson BD, Hembree KJ, Shrestha A. 2013. 62:16–22. nisms of resistance to bispyribac-sodium in an Echino- Glyphosate resistance is more variable than paraquat Vencill WK, Nichols RL, Webster TM, et al. 2012. Herbicide chloa phyllopogon accession. Pestic Biochem Physiol resistance in a multiple-resistant hairy fleabane (Conyza resistance: Toward an understanding of resistance de- 68:156–65. bonariensis) population. Weed Sci 61:396–402. velopment and the impact of herbicide-resistant crops. Gaines TA, Shaner DL, Ward SM, et al. 2011. Mechanism of Okada M, Hanson BD, Hembree KJ, et al. 2013. Evolution Weed Sci 60 (Special Issue):2–30. resistance of evolved glyphosate-resistant Palmer ama- and spread of glyphosate resistance in Conyza canaden- Yasuor H, Milan M, Eckert JW, Fischer AJ. 2011. Quinclorac ranth (Amaranthus palmeri). J Ag Food Chem 59:5886–9. sis in California. Evol Appl 6:761–77. resistance: A concerted hormonal and enzymatic effort Gibson KD, Fischer AJ, Foin TC. 2001. Shading and the Okada M, Hanson BD, Hembree KJ, et al. 2014. Evolution in Echinochloa phyllopogon. Pest Manag Sci 68:108–15. growth and photosynthetic responses of Ammannia coc- and spread of glyphosate resistance in Conyza bonarien- Yasuor H, Osuna MD, Ortiz A, et al. 2009. Mechanisms of cinnea. Weed Res 41:59–67. sis in California and a comparison with closely related C. resistance to penoxsulam in late watergrass (Echinochloa canadensis. Weed Res (in press). Gibson KD, Fischer AJ, Foin TC, Hill JE. 2003. Crop traits phyllopogon). J Agr Food Chem 57:3653–60. related to weed suppression in water-seeded rice (Oryza Orloff SB, Putnam DH, Canevari M, Lanini WT. 2009. Yasuor H, TenBrook PL, Tjeerdema JS, Fischer AJ. 2008. sativa L). Weed Sci 51:87–93. Avoiding Weed Shifts and Weed Resistance in Roundup Response to clomazone and 5-ketochlomazone by Echi- Ready Alfalfa Systems. UC ANR Pub 8362. Oakland, CA. Hanson B, Fisher A, Shrestha A, et al. 2013. Selection Pres- nochloa phyllopogon resistant to multiple herbicides in sure, Shifting Populations, and Herbicide Resistance and Pimentel D, Zuniga R, Morrison D. 2005. Update on the Californian rice fields. Pest Manag Sci 10:1031–9. Tolerance. UC ANR Pub 8493. Oakland, CA. 6 p. environmental and economic costs associated with Yuan JS, Tranel PJ, Stewart Jr CN. 2007. Non-target-site alien-invasive weeds in the United States. Ecol Econ herbicide resistance: A family business. Trends Plant Sci Hanson BD, Shrestha A, Shaner DL. 2009. Distribution of 52:273–88. glyphosate-resistant horseweed (Conyza canadensis) and 12:6–13. relationship to cropping systems in the Central Valley of California. Weed Sci 57:48–53.

152 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 MAINTAINING LONG-TERM MANAGEMENT

Over 35 years, integrated pest management has reduced pest risks and pesticide use by Peter B. Goodell, Frank G. Zalom, Joyce F. Strand, Cheryl A. Wilen and Karey Windbiel-Rojas

Pests and their interactions with crops, ecological landscapes and animals are in con- ntegrated pest management (IPM) is tinuous flux — they are never static. Pest severity increases or decreases depending a systems approach to pest manage- ment. Because of the diverse situations on environmental conditions and changes in production or pest control practices. Pest I in which pests occur, what constitutes management is made even more challenging by exotic and newly invasive pests. Over IPM best practices may vary with time, its 35-year history, the UC Agriculture and Natural Resources Statewide IPM Program location and other circumstances. IPM has supported research and extension that has decreased risks of crop losses, improved considers each available control tactic — for example, cultural, biological, chemi- treatment programs for invasive and endemic pests, and reduced the use of pesticides cal — and often applies a combination of and their impact on the environment and human health. Its publications are widely tactics to enhance overall effectiveness used among growers, pest control advisers, research institutions, state agencies, ag- and reduce reliance on any single tactical ricultural organizations and gardeners; and integrated pest management has been approach. It relies on extensive knowl- edge of the pest, the crop and the environ- adopted statewide in agriculture, as well as in managed landscapes and urban areas. ment in which it exists. Regularly and frequently monitoring the status of a pest, its natural enemies and the site is funda- mental to IPM decision making. In 1979, the California legislature Elena Zhukova Elena provided funding to the UC Division of Agricultural Sciences (now Agriculture and Natural Resources, ANR) to estab- lish the UC Statewide Integrated Pest Management Program (UC IPM). The broad goals of the original program have remained consistent: • Increase use of ecologically based integrated pest management programs. • Provide leadership in IPM, including building coalitions and partnerships that link with communities and public agencies. • Increase the predictability and ef- fectiveness of pest management techniques. • Develop science-based pest manage- ment programs that are economically and environmentally sustainable and socially appropriate. • Protect human health and the environ- ment by reducing risks caused by pests and pest management practices.

Since 1980, UC IPM scientists have worked with other ANR scientists to

In 2001, UC IPM and the Center for Invasive Species Research established a grant program to support research of exotic and invasive pests and diseases such as European grapevine moth, glassy-winged Online: http://californiaagriculture.ucanr.edu/ sharpshooter and Pierce's disease. Lab assistant Emily Kuhn checks a pheromone trap for European landingpage.cfm?article=ca.v068n04p153&fulltext=yes grapevine moth in a vineyard at UC Davis Oakville Research Station, Napa County. The moth, which is endemic to Mediterranean Europe, was first discovered in California in 2009. doi: 10.3733/ca.v068n04p153

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 153 conduct research on specific pests and A stable IPM system can also be up- timeframe of UC IPM. Most of the invad- pest systems and develop economically set by the introduction of an exotic pest. ers, however, have been established for a feasible and environmentally sound Opportunities for UC scientists to conduct half century or more. IPM programs. These programs have research on the management of exotic Development of IPM programs for key been extended to California growers by pests in California are extremely limited pests, whether endemic, invasive but long IPM advisors and other UC Cooperative due to regulated early response programs established, or more recently introduced, Extension (UCCE) advisors. by federal and state agencies. However, shares many commonalities. It requires an Experience has shown that develop- once these invaders become established, understanding of the pest's biology and ing and implementing an IPM program they can be studied as part of the ecosys- interactions with the crop to develop an is only the first challenge. Maintaining tems they have invaded, and managed in integrated approach that favors the crop an IPM program in which the pest and an IPM systems framework. While virtu- over the pest. To be effective, program its damage are managed economically ally all of the pests for which UC IPM has development must include the skills and and with minimum risk to the environ- guidelines are established in California, a knowledge of other UC researchers and ment and human health is often not eas- significant number of them, 40% or more, the results must be distributed widely. ily achieved. One goal of a mature IPM are not endemic but were invaders that ac- This challenge is largely met through system is to establish equilibrium within companied the movement of people, food competitive grant funds, production of the ecosystem, such that frequent chemi- or plant material into the state. Some of educational materials and demonstra- cal intervention is not required. This goal these pests, including sudden oak death, tion of new practices in local fields and is rarely achieved, however, due to the thousand cankers disease, giant reed, orchards. dynamic nature of pests, horticultural Sahara mustard, ash whitefly, sweetpo- UC IPM overview practices, crop values, new pest control tato whitefly biotype B, glassy-winged technologies, new regulations and the sharpshooter, olive fruit fly and spotted UC IPM was built upon the successful range of possible ecological landscape wing drosophila, were first detected and land-grant university research and ex- interactions. became problematic after 1980, within the tension model. Beginning in 1979, UCCE

Publications provide a foundation of IPM practices IPM’s publications and website (ipm.ucdavis.edu) have Pest Management Guidelines UC greatly contributed to the statewide adoption of IPM prac- (PMGs), Pest Notes, Quick Tips and tices by growers, landscape professionals and gardeners. To date, Pest Alerts. There are 47 PMGs rep- there are 19 books in print, and the website has multiple layers of resenting 65 crops and crop groups information, including pest management guidelines for 65 crops. available on the UC IPM website. The Together, the materials present a foundation of IPM practices for Cal- guidelines provide brief descriptions of ifornia crops and urban settings. They are broadly cited in technical a pest’s biology; damage symptoms; and monitoring support; plus biological, cultural and chemical control practices; options for organic production; and illus- trations for diagnostic purposes. Since 2000, the Pest Notes have ad- dressed pests in urban and landscape set- tings, with 166 Notes currently available. Pest Alerts are brief overviews that high- light new pests invading California. Quick Tips are based on Pest Note subjects but provide summaries for easy reference. The PMGs and Pest Notes also contain information on pests of journals, agency reports and nontechnical articles, and the practices quarantine concern for exports, such as the oriental fruit moth for they detail have also been adopted by agricultural organizations stone fruit exports to Mexico, and the Fuller rose beetle for citrus and used in many self-assessment and certification programs (e.g., exports to Japan; IPM management options are in- Lodi-Woodbridge Wine Grape Commission, San Joaquin Sustainable cluded for these insects. Farming Project). To see the full range of UC IPM products, visit ipm. Pest identification and monitor- ucdavis.edu/IPMPROJECT/pubs.html. ing cards. Available for grapes, tree Manuals and books. IPM manuals have been developed and crops, vineyards and residential updated for 17 crops, providing information on pest biology and landscapes, these pocket-sized, nonchemical management of important pests, as well as other laminated cards have high-quality management tactics. Other reference books include IPM in Practice photos and a brief description to aid in and Handbook of Natural Enemies. identifying pests. c

154 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 professionals were hired to consolidate, test and deliver applied research find- ings on pest management to end-users. The program included a computer net- work to process and disseminate data and information required for effective IPM programs, and a designated writing staff to produce IPM manuals and other documents that contained practical infor- mation for growers and other pest man- agement decision makers. Until 2009, UC IPM sponsored a competitive research grants program, which generated new IPM knowledge and practices to address gaps in pest management systems and improve upon Clark Jack Kelly existing practices; it supported more than 450 IPM-related projects. By 1990, at the conclusion of UC IPM’s first decade, 578 publications had been produced based on Ash whitefly (Siphoninus phillyreae), project-funded research. A 1989 survey initially worked with ANR scientists a pest of ornamental indicated that 36% of the principal inves- to develop models to predict potential trees, was first tigators found evidence of a reduction in damage (e.g., the alfalfa weevil model) detected in California pesticides as a result of UC IPM–funded based on pest and weather scenarios. To in 1988. UC IPM– sponsored research research (Grieshop and Pence 1990). improve disease and insect forecasting in at UC Riverside Some of the notable successes from the field, statewide computing networks resulted in a successful UC IPM–sponsored research involved were introduced in the mid-1980s to in- biological control program. Above, then-recent invaders, for example, the ash corporate data from California weather researcher Tom Bellows whitefly. A pest of ornamental trees first networks into the models. In recent years, examining an ash tree detected in California in 1988, the ash web designers have created platforms for for ash whitefly. Right, whitefly became a considerable nuisance delivering IPM information and promot- Clitostethus arcuatus adult (bottom), a for homeowners and businesses because ing IPM practices statewide, nationally natural predator of of the sticky film that covered everything and internationally. ash whitefly, and ash underneath an infested tree. A competi- To ensure IPM practices are adapted whitefly adult (top) tive grant was provided to researchers to local conditions, IPM advisors have on leaf, UC Davis

Arboretum. Clark Jack Kelly In recent years, web designers have created platforms for delivering and extension projects were developed IPM information and promoting IPM practices statewide, nationally by cross-disciplinary teams of key sci- and internationally. entists from all three UC campuses with colleges of agriculture (Davis, Berkeley at UC Riverside to study its biology and been distributed throughout the state to and Riverside) and UCCE academics from support foreign exploration for biological implement IPM through field research critical counties in which the crops were control agents. The research resulted in a and extension. One of their key roles is to produced. Each team focused their re- permanent and successful management support local production farm advisors search efforts on the biology of the pests program utilizing biological control as its in integrating the latest pest management and natural enemies in the cropping sys- primary management approach. practices into local cropping systems. tem and the crop plant’s development to In the early 1980s, technical writers Equally important, IPM advisors commu- better understand the relationship among and editors developed comprehensive nicate locally identified pest management those three key elements of pest popula- IPM manuals for 15 crops and created needs to campus-based researchers. tion growth. Key research topics included pragmatic and easily updatable guide- improved decision making, better timing Foundation of UC IPM, 1980 to 1986 lines for managing pests of specific crops. of pesticide intervention, increased un- Other innovative publications followed, During the formative years of UC derstanding of crop and pest interactions, including additional books, Pest Notes, IPM, nine major crops were highlighted and alternative pest control approaches. and pest identification and monitoring for IPM research and extension: alfalfa, Crop modeling was emphasized to cards (see sidebar, page 154). almond, cereals, citrus, cotton, grapes, increase knowledge of environmental Computing and network technology rice, tomatoes and walnuts. The selection influences on pest and crop dynamics. A have been critical to UC IPM’s informa- of these crops was largely based on their crop model is a mathematical simulation tion delivery. Computer programmers value, acreage and pesticide use. Research of the growth and development of a plant

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 155 Jack kelly Clark Jack kelly Clark 156 T IPM footprint urban andcommunity UC IPM increases its sionals. sionals. profes management pest structural and centergarden staff, landscapers and for retailand in newsletters nursery blogs/UCIPMurbanpests/index.cfm ( blog Urbanthe Landscape in Pests the are on frequently posted rent IPM on and updates articles news, staff. cur nursery audiences To keep Master Gardeners, and retail schools and training materialsvideos for UC developed for urban audiences include and other products pests, landscape information nearly on 1,000 and home IPM website (ipm.ucanr.edu) contains UC The and invasivescapes, pests. waters, IPM and land in structures residential runoff in surface pesticide water on from quality impact pests, use, natural of protection enemies of pesticide of dressed include reduction ment to this area. Issues currently ad reinforces program’s commit and the codifies UC IPM’s IPMurban resources IPM program Community and Urban alike. sionals educate professionals and nonprofes UC IPM increasing began resources to man health and air and water quality, hu on well. impacts the Recognizing garden nonprofessionals increased as and home and tenance professionals, controlpest main landscape operators, cities grew, use by structural pesticide However,andcrops. fiber Californiaas Officially established2007,Officially in the CALIFORNIA search food was on and extension originalhe focus UC IPM’s of re c

AGRICULTURE • VOLUME ucanr.edu/ - - ) ------68 , NUMBER New focus, new pests, 1986to 2000 Pence (1990). in found be can supported sion projects - exten and of research complete listing A programs. by UC IPM–sponsored developed information and publications (PCAs) advisers control were using pest 43% 43% that and of of growers revealed Pencevey and by conducted Grieshop tomato. 1989 in The pests sur caterpillar for and almonds and cotton in mites for spider sampling binomial including to use, easy and reliable,to be accurate have yield. on can pact pests im the by predicting interactions pest of crop– understanding the aid greatly models Such incorporated. to be pests and environment by the caused stress grape) for allows cotton, (alfalfa, that predatorymidgeforAphidoletes control ofrosy appleaphidinContra Costa County. 1999 focused control. onbiological Farm Advisor JanetCaprile reaches into trellised apples to release ofIPMA survey research grant awardees found between that conducted 1989and 38%ofprojects public spaces, natural areas and animal animal and areas public spaces, natural sites, as noncrop such in more and crops, many on diseases and pests studying for opportunity the expanded change This projects. to practice-based projects crop-based from changed was direction of UC crops, set awider IPM’s in sues is pest order to address In Agriculture. of and Food Department California and of Pesticide Regulation Department California as such public agencies and Berkeley,from Riverside, and Davis of PCAs, growers, faculty UC campus consisted Stakeholders focus. extension and program’s the to review research UC and IPM staff of stakeholders ing Sampling methodology was refined refined was methodology Sampling In 1986, In UC IPM convened ameet 4 - - - - and other crops, such as melons, in the the melons, in as such crops, other and of cotton production for the ated acrisis tabaci Bemisia of variant B, a whiteflygenetic biotype of sweetpotato appearance example, the For IPM programs. existing affecting were that of new pests management the growers, and PCAs with collaborations local with and program grants petitive its com through to address, IPM began procedures. trol - con pest nonchemical produced entirely projects 30% of the Overall, pesticides. botanical and microbial investigated 13% and enemies natural of indigenous use and control biological on focused 1990s, the 38% projects of the during toward pesticides climate regulatory the in changes Reflecting control. pest of to improve efficacy the undertaken were projects of the two-thirds and use pesticide toward reducing directed 1989 1999 between and were projects of the three-quarters almost reported (2000) Shouse and byawardees Klonsky agents orbiotic chemicals. of use biorationale and control cultural control, biological as such approaches management of nonchemical use the ing (appliedmies improv fieldecology)and ene natural and crops pests, between of relationships understanding the ing support, increas decision treatment and monitoring pest improving including ics top on were funded of projects variety awide period, this During agriculture. It was during this period that UC that period this It during was grant of IPM research A survey , in the early 1990s, the cre , in ------

Jack Kelly Clark Imperial Valley and the southern San raptors. Since IPM is only one component Now in its fourth decade, UC IPM Joaquin Valley. The existing manage- necessary for environmental research continues to collaborate successfully with ment program was insufficient to prevent on pesticide mitigations, a diverse group UC campuses, UC Cooperative Extension, late-season outbreaks of the new biotype of scientific expertise needed to be as- commodity organizations and govern- that resulted in unacceptable cotton lint sembled. UC IPM provided leadership mental agencies. It provides a platform covered in sticky honeydew. Research by in coordinating projects to identify and for the organization, coordination and scientists from UC Davis, UC Riverside extend mitigation practices and alterna- leadership needed for addressing pests and UCCE, partially funded by UC IPM, tives to the high-risk organophosphate and pest-related issues that threaten and extension of new management tactics insecticides. The use of these insecticides California crops, rangeland, public spaces coordinated by IPM advisors ultimately subsequently declined dramatically and residential landscapes. c resulted in the whitefly’s successful man- across California orchard crops as grow- agement. Other newly discovered invad- ers turned to winter orchard floor man- ers targeted by UC IPM funding included agement, reduced-risk insecticides and blue gum psyllid, Russian wheat aphid alternative treatment timings. P.B. Goodell is UC Cooperative Extension (UCCE) Advisor, IPM, Kearney Agricultural Research and Extension and giant whitefly on urban plants. Publication of the Natural Resources Center; F.G. Zalom is Professor, UCCE Specialist and Defense Council white paper “More IPM Changing regulations, more new pests, Entomologist, Agricultural Experiment Station, UC Davis; Please” (Hamerschlag 2007) focused 2000 to 2012 J.F. Strand is IPM Coordinator Emeritus; C.A. Wilen is Area public attention on the role of IPM in IPM Advisor, San Diego County; and K. Windbiel-Rojas In 2001, UC IPM expanded its role in the conservation of natural resources. is Associate Director for Urban & Community IPM and addressing exotic and invasive pests by In response to the white paper, UC Area IPM Advisor. collaborating with the Center for Invasive IPM began working closely with USDA Species Research at UC Riverside through Natural Resources and Conservation its UC Exotic/Invasive Pests and Diseases Service (NRCS) to develop an IPM Research Program to establish a competi- training program for NRCS staff. The References tive grant program funded through the training emphasized IPM practices that Brewer MJ, Goodell PB. 2012. Approaches and Incen- tives to Implement Integrated Pest Management predecessor of USDA’s National Institute mitigate the impacts of pest management which Addresses Regional and Environmental Issues. for Food and Agriculture. From 2001 to activities on soil, water, air, plants and Ann Rev Entomol 57:41–59. 2009, 102 projects were supported that ad- animals. This partnership with NRCS in Grieshop JI, Pence RA. 1990. Research results: State- wide IPM’s first 10 years. Calif Agr 44(5):24–6. dressed specific exotic and invasive pests California provided an opportunity to Hamerschlag K. 2007. More Integrated Pest Man- and diseases, including European grape- increase IPM adoption by linking activi- agement Please: How USDA Could Deliver Greater vine moth, glassy-winged sharpshooter ties to NRCS-recognized practices for cost Environmental Benefits from Farm Bill Conservation Programs. Natural Resources Defense Council Issue and Pierce’s disease (see pages 125–141). sharing (Brewer and Goodell 2012). For Paper, Feb 2007. 23 p. www.nrdc.org/health/pesti- Since the emergence of a new pest may example, as part of NRCS whole farm cides/ipm/contents.asp. result in pesticide applications that are resource planning, the inclusion of an Klonsky K, Shouse B. 2000. IPM research profiled: 10- detrimental to an established IPM system, IPM plan was encouraged to identify po- year trends. Calif Agr 54(6):20–1. Pence B. 1990. Bibliography of Research, 1980–1990. the funded projects studied the effects tential mitigation activities related to pest Publication 10. University of California Statewide of those applications, with results often management. Integrated Pest Management Project. 57 p. leading to useful revisions of the UC IPM guidelines. Information on exotic and invasive pests, including management guidelines, is now disseminated in all UC IPM materials and at ipm.ucdavis.edu/ EXOTIC/index.html. Concern about the impact of pesticides Over 40% of the on humans and the environment intensi- pests for which UC fied during the 1990s. For example, legis- IPM has guidelines were invaders lation such as the Food Quality Protection that accompanied Act of 1996 resulted in increasingly the movement of stringent enforcement of environmental people, food or regulations. UC IPM worked closely with plant material into California. Bagrada growers and regulatory agencies to iden- bug (Bagrada tify and implement appropriate manage- hilaris), an invasive ment strategies to decrease risks posed pest species native to Africa, attacks from pesticide use. Of particular note vegetable crops and was the reduction of the use of organo- ornamental plants. It phosphate insecticides as dormant sprays was first found in Los in orchards during sensitive periods of Angeles County in 2008, and since then rainfall and fog to protect surface water has spread north to quality, air quality and wildlife, including 19 counties. County Angeles Los Arakelian, Gevork Goodell Peter

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 157 REVIEW ARTICLE: E-EDITION ▼ E-Edition

The cost of the glassy-winged sharpshooter to California grape, citrus and nursery producers

by Karen M. Jetter, Joseph G. Morse and John N. Kabashima

In the late 1990s, widespread outbreaks of Pierce’s disease in Clark Jack Kelly grapevines were linked to transmission via the glassy-winged sharpshooter (GWSS), threatening California’s multibillion-dollar table, raisin and wine grape industries. Government agencies responded to the crisis by implementing two control programs to manage GWSS. We analyzed the long-term economic impact of these two programs on citrus, grape and nursery producers. The net economic effects on all citrus producers and on grape producers in the southern San Joaquin Valley were insignificant, while all grape producers in the Temecula Valley saw an average increase in annual production costs of about $13.04 an acre. Based on our survey of nurseries in Southern California, approximately 11% had an infestation in 2008 and 2009, but only 3.0% in 2010. Average losses to nurseries per GWSS infestation were about $12,238. Nursery producers also undertook a variety of pest con- trol methods to prevent infestations and plant losses, and to meet quarantine regulations. Average annual per-acre costs of these approaches were $2,975 for barrier methods to prevent GWSS from entering a premises, $1,032 in pesticide controls and $1,588 To contain the spread of PD, the California Department of Food and Agriculture placed a quarantine on the movement of plant material from GWSS-infested for in-house monitoring. areas to GWSS-free areas within California. Above, discoloration of grape foliage caused by PD and sunburn on fruit in a Sonoma County vineyard.

n 1989, a pest new to California, the glassy-winged sharp- the late 1990s, were linked to transmission of the causal bacte- Ishooter (GWSS), was collected in Irvine. Since then, it has rium, Xylella fastidiosa, via GWSS. been identified throughout Southern California and has spread At the height of the outbreak in the Temecula Valley, about into the southern San Joaquin Valley, including Kern County, 200 acres, or 10% of the total grape acreage in the Temecula parts of Fresno and southern Tulare counties, and to the coastal Valley, was lost to PD (Siebert 2001). These outbreaks were fol- counties of Ventura, Santa Barbara and San Luis Obispo. The lowed in 2001 by widespread PD outbreaks in grapes in parts of main commercial hosts for GWSS are citrus, grapes, almonds the southern San Joaquin Valley, raising concerns for the health and alfalfa. GWSS overwinters in citrus, avocados, riparian veg- and economic viability of California’s nursery industry and etation and on several ornamental plants, such as crape myrtle. multibillion-dollar grape industry (USDA NASS 2011). Shortly As grapevines and almond trees thereafter, the California Department of Food and Agriculture leaf out in the spring and sum- (CDFA) changed GWSS’s rating from a “C” rated pest (an organ- mer, GWSS moves onto those ism not subject to state-enforced action except to provide for hosts. Feeding by GWSS generally pest cleanliness in nurseries) to a “B” rated pest (an organism Jack Kelly Clark Jack Kelly does not result in economic losses, of known economic importance subject to eradication, contain- and it was initially treated as a ment, control or other holding action at the discretion of the harmless pest. However, in the individual county agricultural commissioner [CAC]). early 1990s, widespread outbreaks Glassy-winged sharpshooter To read full text of this peer-reviewed article, go to the current issue at (Homalodisca vitripennis) caused of oleander leaf scorch in South- http://californiaagriculture.ucanr.edu widespread outbreaks of Pierce’s ern California, followed by signif- disease in Southern California. icant outbreaks of Pierce’s disease Online: http://californiaagriculture.ucanr.edu/ Initially, before it was identified as a vector of the disease, it was (PD) in table, raisin and wine landingpage.cfm?article=ca.E.v068n04p161&fulltext=yes treated as a harmless pest. grapes in the Temecula Valley in doi: 10.3733/ca.E.v068n04p161

158 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 2014 index

The following peer-reviewed research articles, and news and editorial coverage, were published in California Agriculture, Volume 68, Numbers 1 to 4 (January– June, July–September, October–Decem- ber), 2014. E = Article initially published online. Back issues are $5 per copy, while supplies last. To subscribe to the journal, order back issues, search the archives or download PDFs of all research articles in full, go to: http://californiaagriculture.ucanr.edu. January–June, 68(1–2) July–September, 68(3) October–December, 68(4)

Research and Review Articles Economics and public policy SIDEBAR: Editors. The Nutriture Platts BE, Grismer ME. Rainfall leaching is Natural resources of People: From The Yearbook of critical for long-term use of recycled water Jetter KM, Morse JG, Kabashima JN. The Agriculture (USDA 1959). 68(1,2):33. in the Salinas Valley. 68(3):75–81. WE Brusati ED, Johnson DW, DiTomaso JM. cost of the glassy-winged sharpshooter Predicting invasive plants in California. to California grape, citrus and nursery SIDEBAR: Coats WJ. 2014. Improved 68(3): 89–95. Land, air and water sciences leaching practices save water, reduce producers. 68(4):161–7. E, EI SIDEBAR: Coats WJ. Eucalyptus fuel Arnold BJ, Upadhyaya SK, Roach J, drainage problems. 68(3):77. dynamics, and fire hazard in the Tumber KP, Alston JM, Fuller KB. Pierce’s Kanannavar PS, Putnam DH. Water Weber E, Grattan SR, Hanson BR, Vivaldi Oakland hills. 68(3):91. disease costs California $104 million per advance model and sensor system can year. 68(1,2):20–9. GA, Meyer RD, Prichard TL, Schwankl reduce tail runoff in irrigated alfalfa fields. LJ. Recycled water causes no salinity or Pest management SIDEBAR: Editors. Early conclusions on 68(3): 82–8. WE toxicity issues in Napa vineyards. 68(3):59– Pierce’s disease. 68(1,2):21. SIDEBAR: Coats WJ. Placement of 67. WE Espino LA, Greer CA, Mutters RG, Thompson JF. Survey of rice storage tensiometers as guides to irrigation SIDEBAR: Coats WJ. Irrigation of Food and nutrition facilities identifies research and education practices. 68(3):87. WE deciduous orchards and vineyards needs. 68(1,2):38–46. Blackburn ML, Bruhn CM, Soederberg Platts BE, Grismer ME. Chloride levels influenced by plant-soil-water Miller L, Ganthavorn C, Ober B. Seniors, increase after 13 years of recycled water relationships in individual situations. SIDEBAR: Editors. Early grain storage and their food handlers and caregivers, use in the Salinas Valley. 68(3):68–74. WE 68(3):63. research. 68(1,2):41. need food safety and nutrition education. 68(1,2):30–7. SIDEBAR: Coats WJ. 2014. Can irrigation with municipal wastewater conserve energy? 68(3):73. News departments Corrections Palin Stein M. The rise of the kiwifruit. Collaborations 68(3):96. Hayden-Smith R, Surls R, Palin Stein M. California milestones. 68(3):52. White H. A look at EIPD Strategic Initiative Adaska JM, Atwill ER, Nader GA. regulators collaborate on European projects. 68(4):105–8. EI Diagnostics in animal health: How UC grapevine moth program. 68(4):125–33. EI Editors. Early conclusions on Pierce’s helps exclude and minimize impact of Goodell PB, Zalom FG, Strand JF, Wilen CA, disease. 68(1,2):52. Outlook livestock pathogens. 68(4): 109–16. EI Windbiel-Rojas K. Over 35 years, integrated Allen-Diaz B. Rebuilding for the next 100 SIDEBAR: Nader GA, Oliver MN, Finzel pest management has reduced pest risks Editorials/editorial overviews years. 68(1,2):6–7. UC JA, Blanchard MT, Stott JL. Solving the and pesticide use. 68(4):153–57. EI Grafton-Cardwell EE, Jones A, Condos N. puzzle of foothill abortion in beef cattle. SIDEBAR: Goodell PB, Zalom FG, UC and the state of California team up Harter T, Dahlke HE. 2014. Out of sight but 68(4):114–5. EI Strand JF, Wilen CA, Windbiel-Rojas K. against invasive species. 68(4):100–1. EI not out of mind: California refocuses on groundwater. 68(3):54–5. WE Bostock RM, Thomas CS, Hoenisch RW, Publications provide a foundation of Napolitano J. ANR and Cooperative Golino DA, Vidalakis G. Plant health: How IPM practices. 68(4):154. EI Extension touch people’s lives. 68(1,2):4–5. Research news diagnostic networks and interagency SIDEBAR: Goodell PB, Zalom FG, Strand UC partnerships protect plant systems from JF, Wilen CA, Windbiel-Rojas K. UC IPM Meadows R. UC Cooperative Extension Parker D. UC ANR applies innovative pests and pathogens. 68(4):117–24. EI increases its urban and community IPM helps Californians use water wisely. research and programs to state’s water SIDEBAR: Bostock RM, Thomas CS, footprint. 68(4):156. EI 68(3):56–8. WE scarcity. 68(3):53. WE Hoenisch RW, Golino DA, Vidalakis G. Hanson BD, Wright S, Sosnoskie LM, Fischer Meadows R. UCCE’s connection to the A broad lab network means greater AJ, Jasieniuk M, Roncoroni JA, Hembree KJ, community continues. 68(1,2):17–9. UC flexibility and better response. Index 2014 Orloff S, Shrestha A, Al-Khatib K. Herbicide- 68(4):121. EI 68(4):159. Warnert J. Unwelcome arrivals. resistant weeds challenge some signature 68(4):102–4. EI Bruening G, Kirkpatrick BC, Esser T, Webster cropping systems. 68(4):142–52. EI Other news RK. Cooperative efforts contained spread SIDEBAR: DiTomaso JM. Importance of of Pierce’s disease and found genetic herbicide resistance in weeds of natural Hayden-Smith R, Surls R. A century of resistance. 68(4):134–41. EI areas. 68(4):149. EI science and service. 68(1,2)8–15. UC Special issue/section key SIDEBAR: Bruening G, Kirkpatrick SIDEBAR: Fennimore S, Smith R, Le Hayden-Smith R, Surls R, Palin Stein M. EI = Endemic and invasive pests BC, Esser T, Webster RK. Coordinated Strange M. Herbicide-resistant weeds California milestones. 68(1,2):8–15. UC and diseases response to PD involves growers, unlikely in vegetable crops. 68(4):150–1. Meadows R. New license plate supports UC = UC Cooperative Extension scientists and government. 68(4):138–9. EI EI youth agricultural programs. 68(3):52. centennial Cooper M, Varela L, Smith R, Whitmer Palin Stein M. Developing Northern WE = Water efficiency D, Simmons G, Lucchi A, Broadway R, California’s first ranch marketing program. E = Article published online Steinhauer R. Growers, scientists and 68(1,2):16. UC

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 159 It is the policy of the University of California (UC) and the UC Division of Agriculture & Natural Resources not to engage in discrimination against or harassment of any person in any of its programs or activities (Complete nondiscrimination policy statement can be found at http://ucanr.edu/sites/ California Agriculture anrstaff/files/187680.pdf ) 1301 S. 46th Street Building 478, MC 3580 Inquiries regarding ANR’s nondiscrimination policies may be directed to Richmond, CA 94804 Linda Marie Manton, Affirmative Action Contact, University of California, [email protected] Phone: (510) 665-2163 Agriculture and Natural Resources, 2801 Second Street, Davis, CA 95618, Fax: (510) 665-3427 (530) 750-1318.

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Available from ANR California Master Gardener Handbook, Second Edition

uring winter’s long nights and long-awaited rains, garden- publications, the new California Master Gardener Handbook has Ders at last can take a moment to reflect on what worked well gone through intensive academic peer review to ensure techni- over the last year and what didn’t. It’s a cal soundness. And like the UC Master time for pruning and planning, and gar- Gardener program, it’s practical and deners are aided this year by UC ANR’s straightforward, with techniques and new California Master Gardener Handbook approaches gardeners can easily under- (2nd ed.). stand and apply in their own garden. Originally a loose-leaf collection of handouts accumulated from years of UC You’ll find valuable guidance on all Master Gardener trainings, the Master aspects of Gardener Handbook was first published as • lawn and decorative landscape care a bound edition in 2002. UC Cooperative • backyard fruit and nut trees Extension Environmental Horticulture • low-water irrigation Advisor Dennis R. Pittenger worked for • vegetable gardening years with an array of other UC profes- • plant pest and disease management sionals and Master Gardener volunteers, • and much, much more combing through program training materials, handouts and notes to bring This new edition is a must-have for together an authoritative, comprehensive every gardener’s bookshelf. reference for California gardeners. To California Master Gardener Handbook say the 2002 release was well-received (2nd ed.), ANR Publication No. 3382, would be an understatement — within 756 pp, $37 two months UC had to order a second printing, and it’s been a steady top-seller ever since. Now, a dozen years later, a new and expanded edition is To order: available: 756 pages of completely revised and updated informa- Call (800) 994-8849 or (510) 665-2195 tion, with new color photos and illustrations. Like all UC ANR or go to http://anrcatalog.ucanr.edu RESEARCH ARTICLE The cost of the glassy-winged sharpshooter to California grape, citrus and nursery producers by Karen M. Jetter, Joseph G. Morse and John N. Kabashima Jack Kelly Clark Jack Kelly

In the late 1990s, widespread outbreaks of Pierce’s disease in grapevines were linked to transmission via the glassy-winged sharp- shooter (GWSS), threatening California’s multibillion-dollar table, raisin and wine grape industries. Government agencies responded to the crisis by implementing two control programs to manage GWSS. We analyzed the long-term economic impact of these two programs on citrus, grape and nursery producers. The net economic effects on all citrus producers and on grape producers in the southern San Joaquin Glassy-winged sharpshooter (Homalodisca vitripennis) caused widespread outbreaks of Pierce’s disease in Southern California. Initially, before it was identified as a vector of the disease, it was treated as a Valley were insignificant, while all grape harmless pest. producers in the Temecula Valley saw an for GWSS are citrus, grapes, almonds and to provide for pest cleanliness in nurser- average increase in annual production costs alfalfa. GWSS overwinters in citrus, avo- ies) to a “B” rated pest (an organism of of about $13.04 an acre. Based on our sur- cados, riparian vegetation and on several known economic importance subject to vey of nurseries in Southern California, ap- ornamental plants, such as crape myrtle. eradication, containment, control or other As grapevines and almond trees leaf out holding action at the discretion of the proximately 11% had an infestation in 2008 in the spring and summer, GWSS moves individual county agricultural commis- and 2009, but only 3.0% in 2010. Average onto those hosts. Feeding by GWSS gener- sioner [CAC]). losses to nurseries per GWSS infestation ally does not result in economic losses, Federal and state agencies responded were about $12,238. Nursery producers also and it was initially treated as a harmless to the crisis by implementing control pest. However, in the early 1990s, wide- programs to manage and contain GWSS. undertook a variety of pest control methods spread outbreaks of oleander leaf scorch In 2000, CDFA placed a quarantine on the to prevent infestations and plant losses, and in Southern California, followed by signif- movement of plant material from GWSS- to meet quarantine regulations. Average icant outbreaks of Pierce’s disease (PD) in infested areas to GWSS-free areas within table, raisin and wine grapes in the Tem- California. Plant material can be fruit, annual per-acre costs of these approaches ecula Valley in the late 1990s, were linked twigs or leaves collected during fruit har- were $2,975 for barrier methods to prevent to transmission of the causal bacterium, vesting, or nursery stock. The quarantine GWSS from entering a premises, $1,032 in Xylella fastidiosa, via GWSS. required that all bulk citrus and grapes pesticide controls and $1,588 for in-house At the height of the outbreak in the moved from an infested area to a clean Temecula Valley, about 200 acres, or 10% one meet one of the following criteria: monitoring. of the total grape acreage in the Temecula surveys show that (1) the grove or vine- Valley, was lost to PD (Siebert 2001). These yard is free of GWSS, (2) fruit harvest was outbreaks were followed in 2001 by wide- done in compliance with methods that n 1989, a pest new to California, the spread PD outbreaks in grapes in parts of will eliminate vectors or (3) postharvest Iglassy-winged sharpshooter (GWSS), the southern San Joaquin Valley, raising treatments were completed to remove the was collected in Irvine. Since then, it has concerns for the health and economic vi- vector (CDFA 2013b). been identified throughout Southern ability of California’s nursery industry The CDFA quarantine for nurseries California and has spread into the south- and multibillion-dollar grape industry required that all plants transported from ern San Joaquin Valley, including Kern (USDA NASS 2011). Shortly thereafter, areas with known GWSS populations to County, parts of Fresno and southern the California Department of Food and Tulare counties, and to the coastal coun- Agriculture (CDFA) changed GWSS’s rat- Online: http://californiaagriculture.ucanr.edu/ ties of Ventura, Santa Barbara and San ing from a “C” rated pest (an organism landingpage.cfm?article=ca.E.v068n04p161&fulltext=yes Luis Obispo. The main commercial hosts not subject to state-enforced action except doi: 10.3733/ca.E.v068n04p161

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 161 GWSS-free areas of the state be shipped Inspection Service (USDA APHIS) imple- with USDA APHIS, infested counties, and under a Blue Tag protocol (Kabashima et mented an area-wide treatment program treatment coordinators. al. 2008). This protocol required that the that involves the coordinated control of In addition to the public programs plant material be visually inspected by GWSS on citrus in infested areas where instituted by USDA APHIS and CDFA, the CAC’s office prior to shipment and citrus is grown in proximity to grapes. the grape producers and nurseries most be held for inspection by the destination In these areas, GWSS are monitored, and affected by PD and GWSS quarantine county’s agricultural commissioner’s when they exceed treatment thresholds, undertook their own private measures office. Counties enforcing the Blue Tag GWSS populations are controlled be- to prevent the spread of the disease restriction were Alameda, Contra Costa, fore they can move into vineyards and and vector. In 2001, grape producers as- Fresno, Lake, Mendocino, Monterey, transmit the PD bacterium. Any citrus sessed themselves a fee of $3 per $1,000 Napa, San Joaquin, Sonoma and Tulare. grove located within one-quarter mile of in revenues to fund research and other Under the Blue Tag protocol, if GWSS a trapped grapevine (i.e., a trap that has activities. As part of this effort, in 2002, were detected in the load at the destina- captured a GWSS) is treated. The excep- the PD/GWSS Board funded a nursery tion site, at the discretion of the CAC, tion is a grove located along the northern treatment reimbursement program in it could be sprayed, rejected and/or boundaries of GWSS infestation in the Ventura County; Riverside County was reloaded on the truck to be transported San Joaquin Valley and the California added in 2008. Both counties’ programs out of the county back to the sender, or to coast. In this case, the barrier is one-half are currently active, with eight to 12 another county not requiring the Blue Tag mile from a trapped vine. Areas with ac- nurseries in Ventura County and one protocol (but only with the permission of tive area-wide programs include Kern nursery in Riverside County receiving the new destination county), or destroyed. County, the Temecula and Coachella val- reimbursements twice a year. To receive Shippers and receivers who violated the leys, and parts of Ventura, Fresno, Madera reimbursement, the CAC must verify that quarantine’s nursery stock regulations and Tulare counties (CDFA 2013a). While the nursery is an active in-state shipper, were also subject to fines. In 2010, 99.99% some citrus producers may benefit from has a GWSS compliance agreement and of the 50,600 shipments of nursery stock the control of GWSS in their groves, it has a high enough GWSS population to shipped under the Blue Tag protocol were was thought chemical treatments might justify treatment. In 2005, CDFA imple- free of any viable life stages of GWSS. also disrupt integrated pest management mented the Nursery Stock Approved Only six shipments were intercepted due control practices, imposing additional Treatment Program (NSATP), a 3-year pi- to egg masses (four), nymphs (one) or costs on the citrus industry. Currently, lot that evaluated whether nursery stock adults (one). CDFA manages the federally funded that was treated just before shipping, with In 2001, the U.S. Department of area-wide program as part of its Pierce’s insecticides that provided 100% control Agriculture Animal and Plant Health Disease Control Program in coordination in research experiments (carbaryl or Jack Kelly Clark Jack Kelly Clark Jack Kelly

Oleander is a GWSS host. The yellow, brown, A yellow sticky trap monitors the GWSS population in an almond orchard. GWSS overwinters in citrus, dying leaf margins are a symptom of bacterial leaf avocados and riparian vegetation and moves into almond orchards and grape vineyards as they leaf out scorch vectored by GWSS. in spring.

162 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 fenpropathrin), would provide the same level of efficacy in real-world conditions. The NSATP pilot was 100% effective, with no viable life stages of GWWS detected during the 3 years of the project, which resulted in qualifying nurseries utilizing the NSATP protocol to ship to noninfested areas without an origin inspection. Even with these control programs, grape producers and nurseries often needed to treat or otherwise manage GWSS, affecting crop production costs. How GWSS control affected private con- trol costs depended on the actual pest treatment costs, plus any changes in cul- tural practices such as pruning, irrigation or nursery management. The net effect of private control costs, however, depended on how any additional control measures Rosen David affected the frequency with which they Applications of insecticides in late fall have avoided disrupting biological control and causing secondary substituted for or reduced current pest pest outbreaks. This GWSS egg mass has been parasitized by a Gonatocerus species parasite. control treatments. Finally, private control costs for grape producers may be affected GWSS control costs for citrus by increases in the rate of PD compared in this analysis reflect those current for to the pre-infestation levels, even with 2007–2008. The first line of defense against the GWSS control. In 2011, to determine the economic ef- spread of PD by GWSS is the USDA fects of GWSS on the ornamental nursery APHIS area-wide control program Measuring the costs of GWSS control industry, we sent an online survey to whereby citrus producers treat orchards To estimate the effects of CDFA and the 114 nursery producers in Southern during the fall and/or spring to prevent USDA APHIS control programs on pro- California who ship under the Blue Tag the buildup of GWSS populations. To con- ducer management decisions and costs, protocol. The survey included questions trol for GWSS in citrus, an application of data was needed on changes in cultural on what type of nursery products they acetamiprid is typically made in late fall, practices and the costs of those changes, produced, whether they had ever had followed by an application of systemic the effect on other pest control decisions, a GWSS outbreak, how outbreaks were imidacloprid in the spring. Imidacloprid and changes in nursery costs in infested treated and what preventative measures is applied at a rate of 0.5 pounds of ac- regions. In November and December they took to prevent GWSS from entering tive ingredient (AI) per acre through the 2008, we held meetings in the southern their premises. The survey was pre-tested irrigation system. Treatments and the San Joaquin Valley and the Temecula with select nursery operators in Southern breadth of the area to be treated are deter- Valley with a UC Cooperative Extension California and final adjustments made. A mined based on monitoring and trapping farm advisor, six pest control advisers total of 37 nursery producers responded. results. Under the public program, citrus (PCAs) and producers, and two program Compared to nurseries that produce producers are reimbursed for the total managers to discuss the area-wide pro- for the Southern California market, the cost of their GWSS treatments, includ- gram and how the establishment of GWSS nurseries that ship under the Blue Tag ing all materials, labor and application affected pest control materials applied, protocol need to be large and more di- costs, and participation in the program is costs and nontarget pests. We obtained verse in order to supply the mass mer- voluntary. additional information on pest control chandiser box stores, retail nurseries and Total costs of production for citrus practices and the current rates of PD in landscape installers. Thus, they have producers under the area-wide program infested areas through phone interviews outdoor, shade house and greenhouse may be affected if treating for GWSS in 2009 and 2010 of 12 PCAs in Southern production at one location. Nurseries that allows producers to forego an existing California and the southern San Joaquin do not ship to counties enforcing the Blue treatment, as GWSS control may control Valley and UC Cooperative Extension Tag protocol do not face the same regula- other citrus pests. Alternatively, treat- county advisors. The costs estimated from tions; consequently, they do not typically ments for GWSS may cause secondary these meetings were compared to UC treat for GWSS. By sales, the nurseries pest outbreaks of nontargeted pests. In Cooperative Extension budgets for grapes that ship under the Blue Tag protocol rep- conversations with the authors, local pro- to determine how pest control treatments resent about 40% to 50% of total sales by ducers, PCAs and managers of the area- changed as a result of the treatments re- Southern California nurseries. The pro- wide program reported that there have quired for GWSS (Hashim-Buckley et al. ducers who responded to our survey have been neither substantial cost savings nor 2007; Peacock et al. 2007a, 2007b; Vasquez a product mix typical of those nurseries secondary pest outbreaks. One reason is et al. 2006, 2007). Costs and prices used that ship under the Blue Tag protocol. due to timing: Late fall control of GWSS

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 163 in citrus typically occurs after beneficial consists of one application of systemic im- in the southern San Joaquin Valley is at insects have exerted control, and pesticide idacloprid annually, right before the first about the same level, or slightly less, than residues decline to negligible levels by the leaves appear in the spring. Applications it was before GWSS invaded. As a result, following year; thus, few secondary pest of systemic imidacloprid are typically we estimate that producers in southern outbreaks are observed. Those who were completed at the maximum rate of 0.5 San Joaquin County had no additional interviewed felt that minor additional pounds AI per acre through the irrigation costs due to changes in the incidence of control of pests by spring treatments was system. The cost of applying imidacloprid PD in their area. balanced by the negative impacts of these was about $50 to $60 an acre in 2007. Since Finally, grape producers interviewed treatments on beneficial species — thus, then, the cost of treating with imidaclo- by the authors reported that they did not there was little net impact. prid has fallen due to competition from incur additional costs due to the quaran- The CDFA quarantine program re- generic products. tine on the movement of grapes. Grapes quires that fruit from infested areas be Treatments for one pest often influence destined for the fresh market are hand- inspected and treated before leaving a how another pest is treated. On grapes, harvested and field packed, meeting the quarantine area to be packed in a GWSS- GWSS treatments also control the varie- quarantine regulations that no plant ma- free county. If GWSS are found in a pro- gated leafhopper and western grapeleaf terial be transported with the fruit. The ducer’s orange shipments, the producer skeletonizer. Treatments for these two movement of bulk grapes did not require bears the cost of treating GWSS in his pests were no longer typically needed, as postharvest treatments, as bulk grape pro- or her grove if the producer did not par- the annual application of imidacloprid re- ducers within an infested area can meet ticipate in the area-wide program plus duced these pest populations below eco- quarantine regulations through shipping postharvest treatments. This aspect of nomically damaging levels. We estimate grapes to processing centers within the the public control program is believed to that the cost savings by producers was infested areas, or by treating vineyards if encourage greater participation by citrus $62 an acre, or about the same amount surveys show the presence of GWSS. producers in helping to control GWSS. At as the costs to apply imidacloprid in the The Temecula Valley. Private treatment the time of our meetings and interviews southern San Joaquin Valley in 2007–2008. of GWSS in grapes in the Temecula Valley with PCAs, no citrus producers were in- Insecticides used to prevent GWSS es- also consists of an annual application of curring these costs in the San Joaquin and tablishment in vineyards also control the imidacloprid. With the imidacloprid treat- Temecula valleys. vine mealybug, which was first found ments, producers in the Temecula Valley in the Coachella Valley in 1994 and has no longer needed to treat for the grape GWSS control costs for grapes since spread throughout several grape- twig borer. As was the case in the San The southern San Joaquin Valley. The growing counties in California, including Joaquin Valley, the cost savings for treat- second line of defense against the spread Kern County in the southern San Joaquin ing secondary pests just about offset the of PD is for individual grape produc- Valley. additional costs of imidacloprid. ers to treat their grapevines for GWSS. Grape producers may also suffer losses Because there is greater GWSS pres- Producers typically apply treatments to if the incidence of PD is higher than it sure in this region, however, some grape provide immediate control in case GWSS was before GWSS became established. producers located near citrus groves enters the field, not because it has been According to the PCAs we interviewed in the Temecula Valley treat vineyards identified in their fields. This treatment during August 2010, the incidence of PD with one or two additional sprays of fenpropathrin in about 5% of the grape acreage per year. Fenpropathrin is applied TABLE 1. Added average annual costs per acre to treat GWSS in the Temecula Valley, 2009 at a rate of 11 ounces per acre, with the cost per ounce equal to $1.62. With two Amount treatments per year, the cost to treat with $ per acre fenpropathrin was $35.64. Custom ap- Cost of fenpropathrin plication costs were an additional $25 per Insecticide applied at 11 ounces per acre two times per year at $1.62 per ounce 35.64 acre per application. The average costs per Application by a custom applicator at $25 per acre 50.00 acre to apply fenpropathrin, prorated to Total cost if fenpropathrin applied 85.64 the 5% of acreage that was treated, were $4.28 (table 1). Cost of extra irrigation Furthermore, the Temecula Valley Water applied on 850 vines per acre × 2 gallons per vine × 6 hours of irrigation at a cost of 12.52 has a drier climate than the San Joaquin $400 per acre-foot Valley. In order for producers to apply im- Labor per acre 5.00 idacloprid when it can do the most good, Total cost if an additional irrigation needed 17.52 a separate irrigation may be required. We held meetings with farm managers Costs prorated and PCAs, who estimated that half the Irrigation prorated to 50% 8.76 time they need to complete a separate ir- Fenpropathrin prorated to 5% 4.28 rigation in order to apply imidacloprid. The additional irrigation was estimated Total additional costs 13.04 at 2 gallons of water applied per vine per

164 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 hour over 6 hours (with an average of 850 vines per acre). At a cost of $400 per acre-foot during the time period covered by this study, the total additional cost to irrigate was estimated to be $17.52 per acre (table 1). Prorated to 50% of the time an additional irrigation was needed, the additional cost was estimated to be $8.76 per acre. We estimated that the total cost of the extra fenpropathrin on 5% of the acreage and extra irrigation on 50% of the acreage was $13.04 per acre per year (table 1). Grape producers in the Temecula Valley had a slightly higher incidence of PD in 2007, at 2% to 3%, up from about 1% before the establishment of GWSS. While there were a few large plots that were infested, PD in grape vineyards tended to be localized. Producers typically pulled vines and replanted instead of removing a whole plot; based on UC Cooperative Extension wine grape budgets for the San Joaquin Valley, the cost to replant about 2% of vines a year was $65 per acre (Hashim-Buckley et al. 2007; Peacock et al. 2007a, 2007b; Vasquez et al. 2006, 2007). We estimate that the total cost of GWSS and PD management was about $78 an acre per year in the Temecula Valley. There were no market effects for Clark Jack Kelly grape producers and consumers from To contain the spread of PD, the California Department of Food and Agriculture placed a quarantine on GWSS establishment in California. The the movement of plant material from GWSS-infested areas to GWSS-free areas within California. Above, discoloration of grape foliage caused by PD and sunburn on fruit in a Sonoma County vineyard. success of the GWSS area-wide control program caused few changes in the costs and juice concentrates pay an assess- that had to destroy plants. In contrast, of production for producers in the south- ment to the PD/GWSS board (PD/GWSS only one nursery had to destroy plants ern San Joaquin Valley, where much of Research Board 2013). In 2001, the assess- in 2010. The total cost of the destroyed California’s table grape and raisin pro- ment was $3 per $1,000 in farm revenues. plants, including wholesale value of lost duction occurs. Additional costs to treat By 2008 and 2009, the rate had fallen to $1 plants, labor and materials, was $97,899, GWSS were offset by cost savings on per $1,000 in farm revenues; in 2010, it fell for an average loss of $12,238 per infested other pests. Although producers in the to $0.75. As of 2009, this assessment had operation (table 2). However, costs varied Temecula Valley incurred higher costs raised a total of $34 million (PD/GWSS widely by nursery from a low of $1,500 of production, with about 1,300 acres Research Board 2013). While cumulatively in 2010 to a high of $35,000 for plants planted in wine grapes, their share of the assessment represents a significant destroyed in 2008 (table 2). The plants total grape production in California was funding source to address the GWSS that were destroyed included broadleaf less than 3%, a share too small to influ- problem, the assessment rate represents evergreens, deciduous flowering trees, de- ence markets significantly. As a result, less than 0.5% of revenues, and again ciduous shade trees, perennial herbaceous the higher costs of production were not there are no market effects to produc- bedding plants, ornamental shrubs and offset by increases in market prices, and ers and consumers due to the cost of the annual bedding plants. Annual bedding the net change in producer revenues was assessment. plants were the plants listed most often by equal to the changes in the costs of pro- the respondents as the type of plant that GWSS control costs for nurseries duction. Given that only producers in the needed to be destroyed either in the nurs- Temecula Valley incurred higher costs of Out of the 37 nursery operators who ery or at the destination. production, we estimate the total increase responded to our survey, eight operations Over 50% of the nursery operators in the annual direct costs to the entire had to destroy plants due to the presence who responded (n = 20) to the question on grape industry in California to be about of GWSS in 2008 and 2009 (table 2). GWSS management applied pesticides to $103,000 per year. Four nurseries (or 11%) of the respon- manage GWSS (table 3). GWSS control oc- Additional costs to grape producers. dents destroyed plants in 2009, the year curred both during plant growth and as a Grape producers of wine, wine vinegars with the greatest number of nurseries preshipment treatment.

http://californiaagriculture.ucanr.edu • OCTOBER–DECEMBER 2014 165 TABLE 2. Nursery costs due to GWSS infestations by place and year, 2008–2010 For both types of control, nursery pro- ducers used a variety of chemical treat- Costs ments, including fenpropathrin, carbaryl, Total acetamiprid and abamectin. The average Respondents observations Average Minimum Maximum cost to treat nursery stock on the premises ...... number ...... $ per infestation ...... was $1,032 an acre. Costs again varied 2010 widely with a minimum cost of $175 an In nursery Were plants destroyed? 37 1 acre and a maximum or $2,159. The pre- shipment treatments were a lower cost per Value of plants destroyed 37 1,500 1,500 1,500 acre. The average cost was $229 per acre, Labor and material costs 37 0 0 0 with a minimum cost of $39 per acre and Total average costs 37 1,500 a maximum cost of $850 (table 3). Our survey also asked questions on At point of sale Were plants destroyed? 37 1 other methods used to prevent GWSS in- Value of plants destroyed 37 0 0 0 festations and plant loss, including barrier Labor and material costs 37 0 0 0 methods to prevent the entry of GWSS (or otherwise manage GWSS) and the inspec- Total average costs 37 0 0 0 tions of traps installed by CDFA. Almost Both Were plants destroyed? 37 1 30% of the operators who responded Value of plants destroyed 37 1,500 1,500 1,500 to the question about methods (n = 22) Labor and material costs 37 0 0 0 used some type of barrier method. The methods used were shade cloths (three), Total average costs 37 1,500 an insect screen (one), sticky traps (one), 2009 oleander hedge (one) or a combination of In nursery Were plants destroyed? 37 4 all methods (one). Because oleanders are a GWSS host, it is probable that the nurser- Value of plants destroyed 37 7,500 0 15,000 ies who use oleander hedges are using Labor and material costs 37 1,950 0 5,500 them as a “trapping” hedge to monitor Total average costs 0 9,450 and treat for GWSS. With a diversity in methods, there was a diversity in costs. At point of sale Were plants destroyed? 37 4 Costs ranged from $750 to $4,660 an acre, Value of plants destroyed 37 2,500 0 5,000 with an average of $2,975 (table 3). Both Labor and material costs 37 125 0 500 the minimum cost and maximum cost for Total average costs 37 2,625 the barrier methods were for shade cloths. Most of the barrier methods used pro- Both Were plants destroyed? 37 4 vided additional protection against other Value of plants destroyed 37 10,000 0 20,000 pests; for example, insect screens protect Labor and material costs 37 2,075 0 6,000 against aphids and thrips. Finally, nursery operators were asked Total average costs 37 12,075 about in-house monitoring of GWSS traps 2008 installed by CDFA. About half of the In nursery Were plants destroyed? 37 3 operators who responded to this ques- tion (n = 22) did some in-house monitor- Value of plants destroyed 37 13,000 0 35,000 ing. Monitoring varied though, from as Labor and material costs 37 1,200 0 3,600 frequently as once a week to as little as Total average costs 37 14,200 every other month. The average cost per acre to monitor was $1,588. The minimum At point of sale Were plants destroyed? 37 3 cost incurred by a nursery was $24 per Value of plants destroyed 37 1,667 0 5,000 acre, and the highest was $7,680 (table 3). Labor and material costs 37 167 0 500 Among the nurseries who responded yes Total average costs 37 1,833 to this question, the two with the highest cost per acre to monitor traps also pro- Both Were plants destroyed? 37 3 duced the greatest diversity of plants. The Value of plants destroyed 37 14,667 0 40,000 number of different plant categories pro- Labor and material costs 37 1,367 0 4,100 duced by these nurseries was twice that of the nursery with the next highest number Total average costs 37 16,033 of plant categories. The nursery that pro- Average over all unique infestations 12,238 duced plants from only one category also

166 CALIFORNIA AGRICULTURE • VOLUME 68, NUMBER 4 had the lowest cost per acre to monitor to the area-wide management programs have been at risk for the spread of GWSS GWSS traps. (San Joaquin Valley, Temecula, Ventura and Pierce’s disease. c and Coachella). These programs allowed Impacts on producers the coordinated treatment of a grape pest The establishment of GWSS and spread by citrus producers in order to prevent of PD fundamentally changed commer- the spread of a deadly grape disease. As K.M. Jetter is Associate Project Scientist, UC Agricultural Issues Center; J.G. Morse is Professor, Department of cial agricultural practices for several table, a result, the net effects in changes in pest Entomology, UC Riverside; and J.N. Kabashima is UC raisin and wine grape producers, as they treatments by commercial grape produc- Cooperative Extension Environmental Horticulture needed to carefully monitor fields for ers were negligible. Advisor, Orange County. both the pest and disease to prevent vine The area-wide programs have not been This study was funded by grants from CDFA’s Pierce’s death. With low GWSS populations, pre- cost-free, however. These programs are Disease Research Program and the Consolidated Central ventive measures undertaken by produc- managed and coordinated by the USDA Valley Table Grape Pest and Disease Control District. ers caused a negligible net change in the and CDFA out of public monies. The profitability of producing grapes. cost of the GWSS area-wide treatment Nursery producers experienced higher program was greater than $20 million costs in some cases. Recurring costs were a year in 2010. In comparison, the aver- incurred for monitoring and preventing age farm-gate value in 2010 of the grape References the entry of GWSS, and certain nurseries and nursery commodities produced in [CDFA] California Department of Food and Agricul- ture. 2013a. Pierce’s Disease Control Program Maps. needed to treat when infestations were California was $3.2 billion for all grapes Sacramento, CA. www.cdfa.ca.gov/pdcp/map_Index. found. Nursery producers also experi- and $1 billion for floriculture production html (accessed July 2013). enced increased costs due to paperwork (USDA NASS 2011). While the benefits of CDFA. 2013b. Pierce’s Disease Control Program. Plant Quarantine Manual. Sacramento, CA. http://pi.cdfa. and coordination of treatments, inspec- the area-wide program are beyond the ca.gov/pqm/manual/pdf/454.pdf (accessed July tions and notifications required by the scope of this analysis, had the program 2013). Blue Tag and NSATP protocols (table 4). not effectively reduced GWSS popula- Hashim-Buckley JM, Peacock WL, Vasquez SJ, et al. The largest impact of GWSS on agri- 2007. Sample Costs to Establish and Produce Table tions to current levels, much of the state’s Grapes: Redglobe in the San Joaquin Valley South. cultural producers occurred in relation multibillion-dollar grape industry would Number GR-VS-07-3. Davis, CA: University of Califor- nia Cooperative Extension. 22 p. Kabashima J, Gutman G, Redak R, et al. 2008. Glassy- TABLE 3. Select average annual nursery costs per acre for GWSS management, 2008–2010 winged sharpshooter nursery approved treatment best management practices. December 2008. Costs In: Kabashima J, Morris G (eds.). Glassy-Winged Sharpshooter Nursery Stock Approved Treatment Yes Manual. 20 p. www.cdfa.ca.gov/pdcp/guidelines. Observations responses Average Minimum Maximum html#Nursery...... number ...... $ per acre ...... PD/GWSS Research Board. 2013. Area-wide FAQs. pdgwss.net/background/area-wide-faqs/ (accessed Treat GWSS on premises 20 11 November 2012). Total costs 20 8 1,032 175 2,159 Peacock WL, Vasquez SJ, Hashim-Buckley JM, et al. 2007a. Sample Costs to Establish and Produce Table Treat for GWSS preshipping 15 9 Grapes: Crimson Seedless in the San Joaquin Valley South. Number GR-VS-07-2. Davis, CA: University of Total costs 15 6 229 39 850 California Cooperative Extension. 22 p. http://cost- Use barrier methods 22 7 studies.ucdavis.edu/current.php. Peacock WL, Vasquez SJ, Hashim-Buckley JM, et al. Total costs 22 4 2,975 750 4,660 2007b. Sample Costs to Establish and Produce Table Have traps used by inspectors 22 18 Grapes: Flame Seedless in the San Joaquin Valley South. Number GR-VS-07-4. Davis, CA: University of Do in-house monitoring of traps 22 10 California Cooperative Extension. 22 p. http://cost- studies.ucdavis.edu/current.php. Total costs 22 9 1,588 24 7,680 Siebert J. 2001. Economic impact of Pierce’s disease Average number of traps used, three; minimum, one; maximum, six. on the California grape industry. In: Proceedings of the Pierce’s Disease Research Symposium. Sac- ramento, CA: CDFA. p 111–6. cdfa.ca.gov/pdcp/ research.html. TABLE 4. Select average annual costs per nursery operationto meet regulatory requirements, 2008–2010 USDA NASS. 2011. Agricultural Statistics, 2011. Washington, DC: United States Government Printing Costs Office. Yes Vasquez SJ, Fidelibus MW, Christensen LP, et al. 2006. Observations responses Average Mininimum Maximum Sample Costs to Produce Grapes for Raisins: Con- ...... number ...... $ per acre ...... tinuous Tray Dried Raisins in the San Joaquin Valley. Number GR-SJ-06-2. Davis, CA: University of Califor- Do own inspections of traps 9 7 111 12 250 nia Cooperative Extension. 22 p. http://coststudies. ucdavis.edu/current.php. Number of inspections per year 9 7 62 2 244 Vasquez SJ, Hashim-Buckley JM, Peacock WL, et al. Total costs 9 7 5,444 24 16,800 2007. Sample Costs to Establish and Produce Table Staff training costs 9 7 1,605 15 10,000 Grapes: Thompson Seedless in the San Joaquin Val- ley South. Number GR-VS-07-1. Davis, CA: University Time spent on paperwork per year 9 6 57 4 150 of California Cooperative Extension. 22 p. http:// coststudies.ucdavis.edu/current.php. Cost of paperwork 9 6 1,433 50 5,000

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