JANUARY-MARCH 2005 ■ VOLUME 59 NUMBER 1 California Agriculture

Beyond organophosphates

University of California | Division of Agriculture and Natural Resources | Research in Agricultural, Natural and Human Resources Environmental laws elicit evolution in pest management

he era of synthetic UC and USDA scientists released a task force report in 1992 organic pesticides entitled Beyond Pesticides: Biological Approaches to Pest Manage- beganT in the 1940s and ment in California (UC DANR Pub. 21512). This report provided brought with it many an overview of possible alternative control tactics without the Robert Van Steenwyk Frank G. Zalom benefits. The new pesti- use of broad-spectrum pesticides, and was produced with Entomologist, Entomologist, cides enabled growers an appreciation for the mounting political pressures on these UC Berkeley UC Davis to produce abundant products because of safety concerns. Two controversial Na- food and fiber, both tional Research Council reports, Regulating Pesticides in Food: economically and predictably. They enabled public health The Delaney Paradox in 1987, and Pesticides in the Diets of Infants officials to control many serious insect-vectored diseases in and Children in 1993, focused attention on dietary risk from the United States and throughout the world. However, the pesticides and on the differential effects of pesticides on vul- universal adoption of synthetic organic pesticides in the nerable groups in the population. These reports questioned 1950s also brought risks. UC scientists soon noted adverse how the EPA established pesticide tolerances, and were drivers impacts from these broad-spectrum pesticides on natural for passage of the Food Quality Protection Act of 1996 (FQPA). biological control agents and developed the concept of The FQPA is the most important regulatory reform yet enacted. “integrated control.” In addition to their adverse effect on Many broad-spectrum pesticide products and uses have been biological control agents, it soon became apparent that pests lost and more are anticipated in the future. could develop resistance to the new pesticides. This resis- The elimination of the uses of many broad-spectrum tance required that increased rates of pesticides be applied pesticides has resulted in the development and registration to achieve acceptable control, exacerbating the problem. of a number of reduced-risk and environmentally benign The publication of Rachel Carson’s famous book, Silent pesticides and control strategies. These new pesticides are Spring, in 1962, brought concerns about the environmental and more pest-specific and less robust in their control and will re- health risks of pesticides to the forefront of public awareness, quire increased vigilance on the part of pest control advisers. and began a national debate. The U.S. Department of Health, The new products are often slower-acting, will control only Education and Welfare established the Commission on Pesti- related pest species, and are more expensive. In addition, cides and Their Relationship to Environmental Health in 1969, resistance to these new materials can occur in populations chaired by UC Davis Chancellor Emil Mrak, to conduct the of many important pest species. Effective reduced-risk pes- first assessment of pesticide risks. The Mrak Commission rec- ticides have not been developed for a number of important ommended the establishment of a governmental mechanism pests. Thus, there could be substantial economic impacts on for assessing the environmental safety of pesticides. California agriculture from implementation of the FQPA. In 1971, President Nixon created the Environmental To address these concerns, the California Department of Food Protection Agency (EPA) by executive order, transferring and Agriculture supported a study to measure the economic pesticide regulation from the U.S. Department of Agricul- impact on the 13 top-valued economic agricultural crops in ture (USDA) to the new agency. Congress soon mandated California if all organophosphate insecticides were eliminated EPA’s charge to evaluate risks and benefits of pesticides by from use. The study, The Economic Impact of Organophosphates in passing the Federal Insecticide, Fungicide and Rodenticide California Agriculture (http://www.cdfa.ca.gov/publications. Act of 1972. Lawmakers had now established a mechanism htm), showed that the elimination of broad-spectrum pesticides for careful evaluation of any pesticide’s environmental and would increase the cost of production, and the amount of in- health risks, and for consideration of more environmentally crease was crop-specific. This report was the stimulus for the benign pest-management alternatives. UC scientists, who publication of this special issue of California Agriculture, in which were already leaders in the development of biological con- UC scientists discuss alternative control measures that they have trol, integrated pest management (IPM) and pesticide toxi- developed over decades of research. cology, became increasingly engaged in national programs The importance of UC maintaining its capacity to respond to identify and develop alternative pest-management strate- to future regulatory issues, introductions of invasive species, gies to broad-spectrum pesticides. They formed alliances vector-related public health issues and economic challenges with their counterparts in federal and California agencies faced by California citizens has never been greater. To meet to develop and implement new pest-management systems these challenges, a new era of cooperation and integration be- and tactics, including both biological and chemical means to tween UC’s Agricultural Experiment Station and Cooperation combat pests. Extension must be implemented in the near future. This re- However, developing and implementing alternatives to organization must be substantial and collegial, and foster the organophosphate pesticides to meet the needs of California’s vertical integration of knowledge development and delivery. highly diverse agriculture, as well as its urban areas and natu- Through the closer integration of these two units, a leaner ral resources, has been and will continue to be a challenge be- and more efficient organization will be positioned to lead cause of decreasing public funding for research and extension. California as it responds to the challenges ahead.

2 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 News departments

4 Letters

California Agriculture 5 Science briefs Galen Rowell/Corbis Pyrethroids in Central Valley News and Peer-reviewed Research published by the Division of Agriculture and stream sediments toxic to Natural Resources, University of California bottom-dwellers VOLUME 59, NUMBER 1 State announces new methyl Executive editor: Janet White bromide use rules; phase-out Managing editor: Janet Byron delayed Under the Food Quality Protection Act of 1996, many Art director: Davis Krauter uses of organophosphate insecticides and other broad- California Agriculture Three of four county spectrum pesticides are being phased out, with impor- 1111 Franklin St., 6th floor anti-GMO measures fail tant implications for California growers; UC scientists are Oakland, CA 94607-5200 exploring a range of alternatives. Shown on this home Phone: (510) 987-0044; Fax: (510) 465-2659 gardener’s shelf are generations of pesticides, some of [email protected] Research articles which have been banned or their uses curtailed. http://CaliforniaAgriculture.ucop.edu

California Agriculture (ISSN 0008-0845) is published quarterly and mailed at periodicals postage rates at Oakland, CA and additional mailing offices. Postmaster: Send change of address "Form 3579" to California Agriculture at the above address. Beyond organophoshates RATES: Subscriptions free upon request in U.S.; $24/year outside the U.S. After publication, the single copy price is $5.00. Orders must be accompanied by payment. Payment may be by check or international money order in U.S. Food Quality Protection Act Various novel insecticides are funds payable to UC Regents. MasterCard/Visa accepted; requests require 7 29 signature and card expiration date. Please include complete address. launches search for pest manage- less toxic to humans, more specific Articles published herein may be reprinted, provided no advertisement for a commercial product is implied or imprinted. Please credit California Agri- ment alternatives to key pests culture, University of California, citing volume and number, or complete date of issue, followed by inclusive page numbers. Indicate ©[[date]] The Regents Van Steenwyk, Zalom Grafton-Cardwell et al. of the University of California. Photographs may not be reprinted without Organophosphate insecticides have al- A number of newly registered insecticides have permission. UC prohibits discrimination against or harassment of any person on the lowed large yield increases, but under the low mammalian toxicity and target specific crop basis of race, color, national origin, religion, sex, gender identity, pregnancy FQPA many will be cancelled. Alternatives pests; however, resistance and secondary pest (including childbirth and medical conditions related to pregnancy and childbirth), physical or mental disability, medical condition (cancer-related are needed to maintain a viable state ag- outbreaks must be managed. or genetic characteristics), ancestry, marital status, age, sexual orientation, ricultural industry. citizenship, or status as a covered veteran (special disabled veteran, recently separated veteran, Vietnam-era veteran or any other veteran who served on active duty during a war or in a campaign or expedition for which a campaign badge has been authorized) in any of its programs or activities. University 35 Microorganisms and their byprod- Policy is intended to be consistent with the provisions of applicable State and 11 Managing resistance is ucts, nematodes, oils and particle films Federal laws. Inquiries regarding the University's nondiscrimination policies may be directed to the Affirmative Action/Staff Personnel Services Director, critical to future use of pyre- have important agricultural uses University of California, Agriculture and Natural Resources, 300 Lakeside Dr., throids and neonicotinoids 6th Floor, Oakland, CA 94612-3550 or call (510) 987-0096. Godfrey et al. ©2005 The Regents of the University of California Zalom, Toscano, Byrne Insect pathogens are potentially effective, but Pyrethroids and neonicotinoids have their commercial use — except Bt — has been Associate Editors become important replacements for or- limited; metabolic compounds from microorgan- Animal, Avian, Aquaculture ganophosphates, but resistance and nontar- isms and oils are widely used in pest control. & Veterinary Sciences get impacts have been already identified. Edward R. Atwill Christopher M. Dewees Kathryn Radke 41 Costs of 2001 methyl bromide Barbara A. Reed Pheromone mating rules estimated for California Economics & Public Policy 16 Richard J. Sexton disruption offers selective man- strawberry industry David Zilberman agement options for key pests Carter et al. Food & Nutrition Amy Block Joy Welter et al. Methyl bromide use restrictions cost strawberry Sheri Zidenberg-Cherr Mating disruption can control insects; growers an estimated $26 million in 2001, Human & Community Development new pheromone-dispersal technologies with costs borne unevenly among counties Marc Braverman Alvin Sokolow are more effective, but insecticides are and different-size growers. Land, Air & Water Sciences sometimes still necessary. David Goldhamer Mark E. Grismer John Letey 47 2004 Index Ken Tate 23 Biological and cultural controls . . . Natural Resources Nonpesticide alternatives can Adina Merenlender suppress crop pests Kevin O’Hara Terry Salmon Mills, Daane Clarification Pest Management Natural enemies of pests play an impor- Janet C. Broome The October-December 2004 cover of Califor- Kent Daane tant role in preventing crop damage; nia Agriculture showed fishermen harvesting Deborah A. Golino cultural practices can also reduce the sus- snow crab in Alaska, a dangerous crab fish- Tim Paine ceptibility of a crop to pests. ery. This identification was omitted from the Plant Sciences caption. California Agriculture regrets this error. Kent Bradford Kevin Day Steven A. Fennimore http://CaliforniaAgriculture.ucop.eduhttp://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH • JANUARY-MARCH 2005 20053 3 Carol Lovatt Letters

WHAT DO YOU THINK? “Crabbing” about Cal Ag cover nal de Pesquisas de Amazonia (INPA) in Manaus, The editorial staff of The October-December 2004 issue of California Ag- Brazil. Several years ago, I met Dr. Rosalee Coelho California Agriculture riculture is, as usual, very interesting and informa- Netto at a conference and decided to donate my welcomes your letters, tive, particularly the Dungeness crab articles. personal library of phytopathology resources to the comments and sugges- tions. Please write to us Your cover picture, however, does not depict institute, which had very little reference literature in at [email protected] or Dungeness crab fishing. More likely the photo is of a its library. I arranged to ship the California Agricul- 1111 Franklin St., 6th snow crab boat — in Alaska or maybe even the Ber- ture magazines, as well as several decades of Plant fl., Oakland, CA 94607. ing Sea! Nevertheless, it is a beautiful, dramatic pho- Disease, Phytopathology and a small library of agricul- Include your full name to. Just looking at it gives me a bit of motion sickness. tural manuals. The crate arrived in good order at the and address. Letters The scene is familiar to me. I did my Ph.D. re- Manaus port in April, but was held up at the docks may be edited for space search at the College of Fisheries and the Institute by a worker strike until August. Finally, all matters and clarity. for Food Science at the University of Washington in were worked out and the shipment is now in the Seattle. To carry out the study I spent many weeks hands of the receiver library. at sea going from Puget Sound as far as the Gulf of In a letter, Dr. Netto of INPA wrote: “The books Alaska. Most of my time was spent aboard a small and journals will be a wonderful and important re- research vessel converted from a trawler. (I almost source for INPA students and researchers.” The acting had my legs cut off by a snapped winch cable that director of INPA, Edinaldo Nelson dos Santos Silva, whipped across the deck.) added, “Your act enriched our library and will help to I have enjoyed reading California Agricul- enlarge the knowledge of our students, professors, re- ture over the years. The topics covered are broad searchers and scholars of the Amazonia region.” and the articles are consistently well written and Franklin Laemmlen County Director & Farm Advisor informative. Your publication is particularly impor- Santa Barbara County tant to me since I have retired and have become a fruit grower — still learning, growing great fruits, trying to make a buck or two and having a lot of fun. Editor‘s response: We are gratified to learn of your do- John G. Chan nation, and impressed that your perseverance paid off. Hilo, Hawaii Because your collection ended in 2004, California Agri- culture has provided a free subscription to the institute’s Editor‘s response: Thank you for your interest in Cali- library (international subscribers normally pay $24 an- fornia Agriculture — and for your correct observation nually to defray postage and handling costs). regarding the October-December 2004 cover. We located this stock photo after searching for an il- lustration depicting the dangerous conditions at sea Editor’s note when the race for crab begins. However, the agency pro- We gratefully acknowledge the efforts of those viding this photo had not documented the identity of the who contributed to the publication of this special crab. We established its identity as snow crab and imme- issue on alternatives to organophosphate insec- diately corrected the omission on our Web site. ticides: Robert A. Van Steenwyk, Cooperative Donation to Amazon research institute Extension Entomologist at UC Berkeley, and Frank G. Zalom, Cooperative Extension Entomologist You will be pleased to learn that a shipment of 50 at UC Davis, who served as co-chairs; California years of California Agriculture magazines (from 1954 Agriculture associate editor Timothy D. Paine, to present) has been received by the Instituto Nacio- Professor and Entomologist at UC Riverside, who oversaw the peer review of manuscripts; and the California Department of Food and Agriculture, which partially funded this issue of the magazine.

New look for nameplate With this issue, the California Agriculture name- plate on the front cover takes on a new look. While using the same typeface, we have slightly enlarged the print and placed it on one line, without italics. We believe this makes it visually stronger and clearer, while increasing flexibility in cover design. Franklin Laemmlen, with his shipment of 5 decades of California Agriculture magazines and other research materials; Rosalee Coelho Netto receiving the shipment for the Instituto Nacional de Pesquisas de Amazonia in Manaus, Brazil.

4 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 Science briefs

Pyrethroids in Central Valley stream sediments toxic to bottom-dwellers

Recent evidence shows that pyrethroids, used Berkeley Weston/UC Donald increasingly as substitutes for organophosphate insecticides (see page 11), accumulate in creek sedi- ments in some locations at levels toxic to freshwater bottom dwellers. Except in the immediate vicinity of their applica- tion, pyrethroids have been considered safe for fish and other organisms that live in the water, but their effect on sediment-dwelling organisms has not been studied, says UC Berkeley biologist Donald Weston. A pipe discharges field runoff into Orestimba Creek near Modesto. Sediment from this creek was found to be toxic to shrimplike bottom-dwellers called Weston and colleagues collected 71 sediment amphipods, most likely because of high levels of pyrethroids. samples from rivers, creeks, sloughs and drainage ditches in the Central Valley and exposed amphi- State announces new methyl bromide use rules; pods and midge larvae to the sediments. These phase-out delayed two organisms are used by the U.S. Environmental Protection Agency (EPA) as indicators of the health In late November 2004, the California Department of of freshwater sediment. Of the sediment samples, Pesticide Regulation (DPR) announced new regulations 20% killed amphipods at an elevated rate relative to limiting the levels of methyl bromide that may remain controls and had concentrations of pyrethroids high in the air for several weeks, the first such subchronic enough to explain the deaths. The study appeared “seasonal exposure” rules in the nation. The rules im- the journal Environmental Science & Technology in pose buffer zones and advance notification for field May (Vol. 38, No. 10). fumigations, as well as other restrictions (see page 41). “We have no data on the effects of the pyrethroids Methyl bromide — a toxic fumigant injected into on resident species,” Weston says. “Such effects are the soil to kill insects, weeds and diseases — is used very difficult to show, although that is an area in widely by American tomato and strawberry farmers, which we are working. However, the test species we as well as in food processing and storage. used are nationally recognized surrogates for resi- The new regulations give the DPR and county ag- dent aquatic life, and their mortality indicates effect ricultural commissioners the authority to ensure that on the resident organisms should be considered.” ambient air concentrations of methyl bromide do not Pyrethroid use in California has risen due to exceed an average daily nonoccupational exposure of increased regulation of organophosphates, which 9 parts per billion (ppb) in a calendar month. In 2001, pose health threats to workers and cause toxic DPR implemented regulations limiting short-term runoff. Agricultural pyrethroid use in California (24-hour) exposures to methyl bromide in the air to no jumped 25% from 1999 to 2002, although, according more than 210 ppb. While maintaining that short-term to Weston, the increase is only half the picture since standard, the seasonal (4-to-8-week) standard of 9 it does not take into account the fact that growers ppb addresses average daily exposures for children or are gradually switching to pyrethroids with greater other individuals deemed most sensitive. toxicity. About 500,000 pounds of pyrethroids were DPR pesticide-use reports show that methyl bro- used in 2002 for nonagricultural uses such as struc- mide applications in California have fallen from more tural and pest control, and landscape maintenance, than 15 million pounds in 1999 to 6.5 million pounds while more than 250,000 pounds were applied to in 2002. Factors contributing to the decline include California farm fields on crops such as cotton, fruit DPR restrictions, research on less-toxic alternatives, and nut orchards, lettuce, alfalfa and rice. and reductions mandated by the federal Clean Air Act Despite this increased use, environmental moni- and the Montreal Protocol, a global treaty regulating toring tends to focus on water sampling, under the ozone-depleting substances that is gradually phasing assumption that sediment-bound chemicals like py- out most uses of methyl bromide. rethroids are unavailable. The current study shows Also in late November, Montreal Protocol negotia- that is likely to be untrue. tors meeting in Prague extended the United States’ Weston advocates best management practices “critical use” exemption for methyl bromide for 1 to reduce the aquatic impacts of pyrethroids. For year, but said the country must cut its use in 2006. instance, practices that reduce soil erosion would (The Bush administration had secured the exemption greatly reduce the offsite transport of pyrethroids. on the grounds that viable alternatives to methyl bro- “In this case, the interests of environmentalists and mide are lacking.) The exemption amounts to a 2.5% farmers are the same,” he says. — Editors increase in allowed usage for 2005, most of which will

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 5 Science briefs

▲ On Nov. 2, voters in Marin County, left, approved a measure banning the planting of genetically modified crops. Similar measures in three other counties failed.

measure were funded largely by farming interests. “People in the county were deciding their own fate, not being influenced by industry outside the coun- ty,” Lemaux says. Anti-GMO supporters say they will try again in San Luis Obispo and Humboldt counties. Accord- ing to published news reports, in Humboldt County supporters ended up opposing the November mea- sure due to flaws in the wording. As in Mendocino County, the authors of Humboldt County’s measure made the mistake of defining DNA as a protein. Moreover, the Humboldt measure could have been interpreted as violating both the state and federal constitutions by, for example, denying offenders the go to California strawberry growers. right to a jury trial, according to Humboldt County “The national adjustment announced for methyl district attorney Paul Gallegos (in a Sept. 8, 2004, bromide use does not affect California restrictions Eureka Reporter article). on the fumigant, which are the toughest in the na- Although the Humboldt County measure failed, tion,” DPR spokesperson Glenn Brank says. “We one of the cities in this county has already jumped into do not expect any significant increases in use given the mix. On Nov. 17, 2004, Arcata’s city council unani- DPR’s limitations on methyl bromide.” mously voted to adopt an anti-GMO ordinance, mak- For more information, go to: www.cdpr.ca.gov/docs/ ing it the only city in California with such a ban. legbills/recntadop.htm (DPR) or http://www.undp.org/ In addition, anti-GMO measures are in the works seed/eap/montreal/ (Montreal Protocol) — Editors in 12 more counties in the state, according to an as- sessment on the UC DANR Statewide Biotechnolo- Three of four county anti-GMO measures fail gy Workgroup Web site (based on information from Measures on the November 2004 ballot to ban the the Organic Consumers Association Web site). They growing of genetically engineered crops failed are Alameda, Lake, Napa, Nevada, Placer, Sacra- in three of four California counties, most notably mento, San Francisco, Santa Barbara, Santa Cruz, Butte, a major rice-growing area that was seen as Solano, Sonoma and Yolo. Of these, only Sonoma an important test case (see “California voters as- County is likely to have an anti-GMO measure on sess anti-GMO initiatives,” October-December the ballot by spring 2005, and this will be a special 2004, page 182). While opponents are claiming vic- election that has not yet been scheduled, says Ryan tory, supporters are downplaying the outcome as a Zinn, national campaigns coordinator of the San short-term setback. Francisco-based Organic Consumers Association, “It could go either way,” says UC Cooperative which is spearheading the anti-GMO movement in Extension biotechnology specialist Peggy Lemaux. California and elsewhere in the country. “It’s too early to tell, we’ll have to see what hap- “The overall strategy in California will likely not pens in the coming year.” change, at least in the near term,” Zinn says. “Down Butte County’s measure lost 61% to 39%, San the road, we will likely set our sights on statewide Luis Obispo’s lost 59% to 41%, and Humboldt’s lost legislation. But we are several years away.” 72% to 28%. In contrast, Marin County’s measure In contrast, on Nov. 30, the Fresno County Board passed 61% to 39%, making it the third California of Supervisors passed a resolution supporting the county along with Mendocino and Trinity to ban use of biotechnology in agriculture. Fresno is one genetically modified organisms (GMOs). of nine Central Valley counties where significant Mendocino County set a precedent in March amounts of genetically engineered crops are grown, 2004 by becoming the first county nationwide to particularly cotton. The resolution was passed at pass an anti-GMO measure. However, this was seen the request of the Fresno County Farm Bureau as largely symbolic because, unlike Butte County, and concludes with the statement: “The County of Mendocino County is not a major agricultural area. Fresno will make every effort to preserve the choice Furthermore, while the opponents of Mendocino of using biotechnology in its county and encourage County’s measure were funded largely by the the establishment of a state or national biotechnol- biotech industry, the opponents of Butte County’s ogy policy.” — Robin Meadows

6 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 REVIEW ARTICLE ▼ Food Quality Protection Act launches search for pest management alternatives

Robert A. Van Steenwyk Frank G. Zalom ▼

Insecticides have long been impor- tant tools for California farmers to combat agricultural pests. By 1995,

organophosphate (OP) insecticides Archives and Museum Collection Center/www.sacramentohistory.org Sacramento such as chlorpyrifos, azinphos-methyl, methamidophos, phosmet and di- azinon accounted for an estimated 34% of worldwide insecticide sales, and they are widely credited with allowing large yield increases in com- In 1910, Bliss S. Brown, professor of botany and horticulture at the University Farm (later UC mercial agriculture. The U.S. Food Davis), demonstrated a spray pump to a pomology class in Davis. Nearly a century later, UC Quality Protection Act (FQPA), signed scientists are researching alternatives to insecticides whose uses are being restricted under the Food Quality Protection Act. into law in 1996, established a new human health–based standard that and nicotine. With the exception of sul- et al. 1959). In addition, organochlo- “reasonable certainty of no harm will fur and pyrethrum, various synthetic rine and cylclodiene insecticides were result from aggregate exposure to the organic insecticides have replaced the widely implicated in adverse effects pesticide chemical residue.” When the inorganic and botanical insecticides. upon wildlife (Carson 1962). As a result, FQPA was passed, 49 OP pesticides In the turbulent years immediately most of these products were eventually were registered for use in pest control preceding and during World War II, banned for use. in the United States; since then, many supplies of the botanical products be- German scientists identified the in- came limited and an effort was made secticidal activity of organophosphorus uses have been canceled and others to identify, synthesize and manufacture compounds the 1930s, but their chemis- are expected to be lost, with particu- replacement insecticides to protect mili- try was primarily exploited for possible lar significance for California growers. tary personnel from insect-borne diseases use as chemical warfare agents. After A number of alternative pest-control and crops from insect pests. Scientists in the war, the organophosphate (OP) products and strategies are available, England and France identified the insec- compounds were developed as insec- with varying degrees of effectiveness ticidal properties of the precursors to or- ticides. The OP insecticides are acutely and cost. Research and develop- ganochlorine and cylclodiene insecticides toxic to mammals, exhibit cholinesterase ment of control measures to replace in 1939. Because their acute mammalian inhibition, have a broad spectrum of toxicity was low and their spectrum of activity against insect pests and have OP insecticides must be pursued to activity against insects was high, the relatively short environmental persis- maintain an economically viable state organochlorine insecticides — which tence. They are much less persistent in agricultural industry. include products such as DDT, dieldrin the environment than the chlorinated and aldrin — were immediately useful hydrocarbons. By 1995, OP insecticides nsecticides have long been important in controlling insect vectors of diseases accounted for an estimated 34% of tools for California farmers to combat (especially typhus and malaria) during worldwide insecticide sales (Casida agriculturalI pests. However, the types World War II. Following World War II, or- and Quistad 1998). Some popular prod- of insecticide products have changed ganochlorine and cylclodiene insecticides ucts include chlorpyrifos (Lorsban), substantially over time in response to became widely used in agriculture. azinphos-methyl (Guthion) and phos- the availability of new chemicals, the Despite their effectiveness, the met (Imidan). They are widely credited development of pest resistance and reg- organochlorine and cylclodiene insec- with allowing large yield increases in ulations addressing environmental and ticides were persistent in the environ- commercial agriculture. health concerns. Prior to World War II, ment, and their effects on nontarget In the late 1940s, methyl carba- most insecticides used by farmers were species resulted in outbreaks of a num- mates were developed as insecticides. inorganic products such as calcium ber of secondary pests or the rapid re- The methyl carbamates exhibited arsenate, lead arsenate and sulfur, or surgence of the target pest through the cholinesterase-inhibition activity simi- botanical insecticides such as pyrethrum suppression of beneficial insects (Stern lar to that of the OP insecticides. Like

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 7 “Food quality” is a misnomer, since FQPA considers all potential findings of a National Research Council pathways by which people may be exposed to pesticides. (1993) report, Pesticides in the Diets of In- fants and Children, which proposed that the OP insecticides, they have a broad including the Food Quality Protection differences exist among segments of the spectrum of activity and are toxic to Act (FQPA) and the Clean Water Act. population in terms of impacts from many nontarget species, particularly The FQPA was unanimously passed by pesticide exposure. beneficial insects as well as wildlife. both houses of the U.S. Congress and The FQPA requires the EPA to reas- They tend to degrade relatively rapidly signed into law by President Clinton on sess all pesticide tolerances. The toler- in the environment, except for aldicarb, Aug. 3, 1996 (US EPA 1996). This piece ance reassessments must consider the which became a problem when it was of legislation has had, and will continue cumulative effects of the aggregate shown to leach in sandy soils and enter to have, a major impact on agricultural exposure from all sources (dietary, groundwater. pesticide use. The FQPA significantly drinking water and residential) of pes- amended two previous laws: the Federal ticides with a common mechanism of The Food Quality Protection Act Insecticide, Fungicide and Rodenticide toxicity. In addition, the tolerance may As a group, both the OP and methyl Act (FIFRA) and the Federal Food, Drug be reduced 10-fold as a safety factor to carbamate insecticides have continued and Cosmetic Act (FFDCA). The FQPA provide additional protection for infants to be widely used in California agri- established a new human health–based and children. This 10-fold safety fac- culture during the past half century. standard that “reasonable certainty of no tor need not be imposed when reliable Growers favor the use of these syn- harm will result from aggregate exposure information indicates that no harm will thetic organic pesticides because they to the pesticide chemical residue.” In this result to infants and children. The law are effective, relatively inexpensive respect, “food quality” is a misnomer, calls for the tolerance reassessments to and have a broad spectrum of activity. since the law considers all potential path- be completed within 10 years (in two Their widespread use, however, has ways by which people may be exposed 3-year increments followed by a 4-year also brought with it environmental and to pesticides when establishing accept- increment), with priority given to pesti- human health concerns, including: pes- able food residue limits. cides that may pose the greatest risk to ticide residues on food, particularly as Previously under FIFRA and FFDCA, public health. The reregistration of all they relate to infants, children and vul- pesticides were registered by the U.S. pesticides registered before 1984 under nerable groups; pesticide contamination Environmental Protection Agency (EPA) FIFRA will incorporate the new health- of rivers and streams via runoff from with the intent to “prevent unreason- based standard of the FQPA. treated fields and orchards; drinking able adverse effects on human health Minor-use pesticides water contamination from the infiltra- or the environment” by establishing tion of pesticides through the soil; and maximum permissible tolerances of a In addition to establishing a new the destruction of wildlife such as birds pesticide residue on food. An important health-based standard of no harm, the of prey as well as the destruction of ben- feature of the FQPA is its special consid- FQPA also provides for the expedited eficial insects and mites. eration of health effects on children and registration review of “reduced risk” These concerns have been addressed other vulnerable individuals. This addi- pesticides. A reduced-risk pesticide has by a number of state and federal laws, tional emphasis in the FQPA reflects the lower human or nontarget organism toxicity, lower potential for environmental contamina- tion and greater potential for increasing the adoption of integrated pest manage- ment (IPM) practices as

Derek and Frances Richardson Derek and Frances compared to conventional insecticides. After a pesti- cide receives a reduced-risk classification, the EPA must make registration review

Courtesy of Lear/Carson Collection, Connecticut College Courtesy of Lear/Carson Collection, decisions within 12 months, considerably faster than for pesticides that do not re- ceive such designation. The act also offers eco- nomic incentives to pesti- cide registrants (usually the manufacturer) who register Rachel Carson (shown, left, in 1951 during her service as a U.S. Fish and Wildlife Service scientist) warned of the environmental impacts of certain pesticides in her 1962 book, Silent Spring. Right, brown ”specialty” or “minor use” pelican populations severely declined during the mid-20th century because of exposure to DDT, which pesticides. Minor uses are thinned their egg shells; the insecticide was banned for general use in 1972. registrations for crops with

8 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 When the FQPA was passed in 1996, 49 OP pesticides were registered for use in pest control in the United States. ANR Communication Services When the EPA released the Revised OP Cumulative Risk Assessment (2002), 14 pesticides had been canceled or pro- posed for cancellation and 28 others had partial use bans. Voluntary and mandated cancellation or restriction on a number of uses for OP insecticides — such as azinphos-methyl, chlorpyri- fos, ethion, ethyl parathion and methyl parathion — has had particular signifi- The Food Quality Protection Act reflects findings of a 1993 National Research Council report, cance for California growers. Pesticides in the Diets of Infants and Children. The law requires an additional 10-fold safety For example, the EPA accepted vol- factor on some pesticide tolerances to provide additional protection for young people. untary label restrictions on azinphos- methyl, which included reducing the less than 300,000 acres in production, the reassessment of OP and methyl car- maximum seasonal rate in pome fruit, which the EPA administrator determines bamate insecticides. lengthening the intervals between last do not provide sufficient economic The OP insecticides bind to the en- application and harvest, and increasing incentive to support registration and for zyme acetylcholinesterase in the central the intervals between an application which there are no effective pesticide and peripheral nervous system. This de- and worker reentry. Restrictions on alternatives, or uses for which the avail- activates the acetylcholinesterase, result- chlorpyrifos included canceling in- able alternatives pose greater human ing in repeated, uncontrolled stimulation season uses on apples and grapes, risks. A pesticide can also receive minor- (firing) at the nerve junctions. The EPA reducing the maximum number of ap- use status if it significantly aids in re- has tentatively considered the OP insec- plications in alfalfa, and increasing the sistance management or improves IPM ticides to act through a common mecha- intervals between an application and systems. The incentives may include an nism of toxicity. While dietary exposure worker reentry for citrus, nuts and stone additional year of exclusive data use, to a particular OP may be low, the simul- fruit. Actions on methyl parathion in- waivers of certain data requirements taneous exposure to multiple OP insecti- cluded lengthening the interval between and expeditious review that could bring cides may result in some segments of the an application and worker reentry, and the product to market sooner. population exceeding acceptable daily canceling most food crop uses (particu- California’s diverse crop production allowances (Byrd 1997). The implementa- larly for commodities consumed by includes many minor uses, and this has tion and ramifications of the OP insecti- children) and all ornamental and public often resulted in fewer available pesti- cides having a common mode of toxicity health uses. All registrations have been cide options for fruit, nut and vegetable has not been clarified at this point. canceled for both ethyl parathion and growers relative to those for the produc- ers of larger acreage field crops such as corn, cotton and soybeans. The FQPA

also set a goal for the EPA to review all Clark Kelly Jack pesticide registrations on a 15-year cycle to ensure that all pesticides meet up- dated safety standards. Additional pro- visions of the FQPA are somewhat less likely to affect California agriculture. Focus on public health risks The reassessment of all pesticide tol- erances by the EPA presents a daunting task for that agency, since there were more than 9,700 in 1996 when the law was enacted. A pesticide tolerance is the amount of allowable pesticide residue on an individual commodity at harvest, and each pesticide (active ingredient) may have many individual tolerances. Therefore, the EPA is giving priority to pesticides that may pose the greatest Pesticide regulation has long been controver- Toxicological research on animals helps to risk to public health, first focusing on sial in California (March 1991 cover shown). inform pesticide regulatory decisions.

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 9 16); and biological and cultural control Jack Kelly Clark Kelly Jack measures (see page 23). The authors of these articles — many of whom pro- vided the pest-management technical expertise for a California Department of Food and Agriculture (CDFA) evalu- ation on the economic importance of OP insecticides in California agriculture (Metcalfe et al. 2002) — broadly review Left, former UC Davis graduate student Till Angermann monitors an autosampler to test the nature of these specific controls, the effects of best management practices for reducing dormant-season organophosphate runoff from orchard crops. Right, closed loading systems are important when handling their advantages and disadvantages certain organophosphate insecticides. compared to other management mea- sures, current uses and prospects for ethion. In addition, the EPA has ac- fective as the OP insecticide and multiple future use. cepted voluntary action on phosmet applications of the alternative insecticide including the cancellation of its uses for are required to achieve adequate pest domestic pets, household ornamentals control. Overall pesticide use may also and fruit trees, and diazinon is no lon- increase if the alternative insecticide is R.A. Van Steenwyk is Cooperative Exten- ger registered for urban uses. It is an- highly pest-specific, so that different in- sion Entomologist, Department of Environ- ticipated that further restrictions on OP secticides must be used for the control of mental Science, Policy, and Management, insecticides including product cancella- a pest complex that could previously be UC Berkeley; and F.G. Zalom is Entomolo- tions will be imposed in the future. controlled with a single OP insecticide. gist, Agricultural Experiment Station, and The research and development of Cooperative Extension Entomologist, Pest control alternatives control measures to replace OP insec- Department of Entomology, UC Davis. The regulatory focus of the FQPA is ticides must be pursued to maintain We gratefully acknowledge the California the reduction of the human health ef- an economically viable agricultural in- Department of Food and Agriculture for fects of pesticides, but it is understood dustry in California. Some pest control financial support in the development of the that economic and environmental measures are becoming widely adopted base document, The Economic Importance consequences will also result from its as OP uses are lost, most notably the of Organophosphates in California Agri- implementation. The quantitative and substitution of chloronicotinyl (neo- culture (Metcalfe et al. 2002), and in publi- qualitative impacts of the modification nicotinoid) and synthetic pyrethroid cation of this special issue. We also thank the or cancellation of OP insecticide use de- insecticides. Further restrictions on the many UC Cooperative Extension Specialists pends on the availability and adoption availability and uses of OP insecticides and Farm Advisors who provided technical of effective alternative control measures. have created market opportunities for expertise in the development of alternative A study of the 13 top-valued California new and novel pesticides, and some scenarios for the specific crops studied. crops having a total market value of of these have found significant mar- References about $10 billion (Metcalfe et al. 2002) ket niches. Nonchemical approaches, Byrd DM. 1997. Goodbye pesticides? The estimated that a total ban of OP insec- perhaps thought to be less effective Food Quality Protection Act of 1996. Regula- ticides on these crops would result in or too costly in the past, are becoming tion 20(4):57–62. a loss of over $203 million for growers preferred choices for some growers. For Carson RL. 1962. Silent Spring. Boston: Houghton Mifflin. 378 p. and consumers. example, while still a small percentage Casida J, Quistad G. 1998. Golden age of Qualitative effects include changes of total U.S. and California production, pesticide research: Past, present, or future? to IPM programs that use OP insec- the organic industry has experienced Ann Rev Entomol 43:1–16. ticides therapeutically, based on pest tremendous growth in recent years. Metcalfe M, McWilliams B, Hueth R, et al. 2002. The Economic Impact of Organophos- monitoring and established treatment The articles in this issue of California phates in California Agriculture. California thresholds. Other qualitative effects Agriculture present pest management Department of Food and Agriculture. Sac- include: positive or negative impacts on measures that can be used singularly or ramento, CA. 41 p + app. www.cdfa.ca.gov/ beneficial arthropods, depending on the publications.htm in an integrated manner as OP replace- National Research Council. 1993. Pesti- specificity and other properties of the al- ment strategies. They include: other cides in the Diets of Infants and Children. ternative control measure; reduced abil- synthetic insecticides that already have Washington, DC: Nat Acad Pr. 386 p. ity to practice resistance management many labeled uses (see page 11); newly Stern VM, Smith RF, van den Bosch R, Hagen KS. 1959. The integrated control con- through the elimination of alternative registered and novel synthetic insecti- cept. Hilgardia 29(2):81–101. modes of toxification and the suppres- cides (see page 29); natural and biologi- [US EPA] US Environmental Protection sion of detoxification mechanisms; and cal toxins that are registered or exempt Agency. 1996. Food Quality Protection Act unintended negative consequences to from tolerances, including genetically of 1996. Washington, DC. www.epa.gov/op- pfead1/fqpa nontarget organisms. modified crop plants (see page 35); US EPA. 2002. Revised OP Cumulative Risk In addition, overall pesticide use may pheromone mating disruption and other Assessment. Washington, DC. www.epa.gov/ increase if the alternatives are not as ef- semiochemical approaches (see page pesticides/cumulative

10 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 REVIEW ARTICLE ▼ Managing resistance is critical to future use of pyrethroids and neonicotinoids

Frank G. Zalom Nick C. Toscano Frank J. Byrne ▼

Synthetic pyrethroids and neonicoti- noids are the most readily available alternatives to the organophosphate and carbamate insecticides. Pyre- throids have become widely used in California, and problems with insecticide resistance and nontarget impacts have already been identi- fied. Neonicotinoids are a new class of insecticide with uses only now being realized. Managing insecticide resistance will be crucial to preserv- ing these new materials as organo- phosphate uses are lost.

nsecticides are often referred to as having a broad or narrow spectrum of activity,I depending on the diversity of pest species they kill. Narrow-spectrum insecticides are generally thought of as Neonicotinoid and pyrethroid insecticides have become important replacements for organo- being less disruptive to biological con- phosphates. UC Riverside staff research associate Greg Ballmer uses a micropipette to extract trol and more environmentally benign xylem from a grapevine in the Temecula Valley. because of their specificity to a few target pest species. In the presence of a complex unique and economically important In a recent report funded by the Cali- pest community, however, use of an in- components of California’s agricultural fornia Department of Food and Agricul- secticide with a high degree of specificity industry. California Department of Pes- ture (Metcalfe et al. 2002), pyrethroid and can require additional applications of ticide Regulation (DPR 2003) reports of neonicotinoid insecticides were identified products that target other taxa. OP usage for 2002 (the most recent data as the most likely alternatives to the OPs. The ability of organophosphate (OP), published) indicate that chlorpyrifos, Even before the OPs are withdrawn, organochlorine and methyl carbamate diazinon and malathion are the most however, the number of applications of insecticides to control a broad range of widely used OPs, while methomyl and insects with a single application led to carbaryl are the only two methyl carba- TABLE 1. Usage of organophosphate and methyl their widespread use for pest control. mates used to any great extent (table 1). carbamate insecticides in California, 2002 With the cancellation of DDT by the The widespread use of these products U.S. Environmental Protection Agency has led to the development of pesticide Pounds a.i.* No. in 1973, followed by bans on the use of resistance in many insect populations Chemical (trade name) applied applications most other organochlorines, agricultural (Roush and Tabashnik 1990). Their use Organophosphates use of the OP and methyl carbamate has also raised concerns about surface- Chlorpyrifos (Lorsban) 1,446,547 36,802 Diazinon 689,603 31,757 insecticides became dominant, with water contamination, resulting in the list- Malathion 619,811 14,653 more than 200 OP insecticides available ing of some California rivers as impaired Phosmet (Imidan) 405,088 7,533 worldwide at their peak. waterways under the U.S. Clean Water Dimethoate (Cygon) 332,543 24,355 OPs and methyl carbamates are still Act. The U.S. Food Quality Protection Methyl carbamates widely registered for use on Califor- Act (FQPA) of 1996 has focused particu- Methomyl (Lannate) 321,476 17,216 Carbaryl (Sevin) 256,030 3,354 nia crops and have been regarded as lar attention on the human risks of ex- * Active ingredient. especially important tools for growers posure to OPs and has already imposed Source: DPR 2003. of vegetable and fruit crops, which are restrictions on their use (see page 7).

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 11 these alternative insecticides is fast ap- in extracts from Chrysanthemum flowers proaching that of the OPs in California (Tanacetum [Chrysanthemum] cinerariae- agriculture (table 2). This is alarming, folium). Research to develop synthetic because it suggests that application of pyrethroids began in the 1940s to en- these materials will continue to increase, hance their efficacy, facilitate large-scale raising immediate concerns about the po- production and improve stability. Al- tential development of resistance. lethrin (Pynemin) was the first synthetic Although non-OP alternatives are al- pyrethroid to be developed and was ready available for most crops, phasing registered in 1949 for public health and out the OPs will require some adjust- urban uses, primarily against mosquitoes ment to current management programs and houseflies. This was considered a as suitable replacements among the first-generation pyrethroid, because it remaining insecticide classes are sought. was chemically similar to a component Pyrethroids are fast-acting insecticides of the natural pyrethrum extract. that kill a broad spectrum of insect Second-generation pyrethroids were pests. They are most often applied as registered in the 1960s to control ur- foliar sprays, by air or ground. For a ban insects. Resmethrin was about 20 number of crop uses, they are serving times more effective than pyrethrum as a direct substitute for an OP. All cur- for controlling houseflies and had lon- rently registered neonicotinoids in Cali- ger residual activity, but like allethrin Top, UC Riverside extension entomologist fornia agriculture are available as foliar was photolabile (containing molecules Nick Toscano examines a Coachella Valley formulations and compare favorably that break down quickly in light) and grapevine trunk for adult and nymph popu- with the OPs in terms of efficacy against therefore unsuitable for outdoor use. lations of vine mealybug, part of a field trial of various treatments. Above, vine mealybug specific groups of insect pests, impacts Permethrin was the first synthetic pyre- damages grapevines, causing them to lose on natural enemies, and worker and en- throid with sufficient photostability for vigor and diminishing grape quality. vironmental safety. agricultural applications. Permethrin and fenvalerate became Pyrethroids increasingly popular the most widely used of the third- cally 10% of the third-generation rates). Pyrethroid insecticides are more stable generation pyrethroids and were The fourth-generation pyrethroids are analogs of the natural insecticides found particularly significant for their broad photostable and relatively nonvolatile, TABLE 2. Usage of synthetic pyrethroid and spectrum of insecticidal so their residual activity is longer than neonicotinoid insecticides in California, 2002 activity at relatively low that of earlier pyrethroids. rates, as well as their Efficacy and cost. Pyrethroids have Pounds a.i.* No. Common improved photostability, become the favored insecticide alterna- Chemical name applied applications agricultural uses which resulted in residual tives to the OPs for growers because in Pyrethroids activity of up to 1 week many cases, they are a direct substitute Bifenthrin 47,443 5,646 Cotton, corn, strawberry, alfalfa on foliage. Permethrin in terms of the range of insects killed, (Pounce or Ambush) is treatment timing and residual activity. Cyfluthrin 57,524 10,258 Alfalfa, cotton, orange, corn still the most widely used Perhaps the only arthropod groups for Cypermethrin and 306,291 8,326 Lettuce, cole crops, pyrethroid in California, which they are not as effective are soil (s)-cypermethrin onion, cotton and is commonly applied insects and mites, and certain insects Deltamethrin 13,001 956 Greenhouse, nursery to leafy vegetables and with piercing-sucking mouthparts. The some tree crops. availability of pyrethroids continues to Esfenvalerate 30,758 24,623 Almond, cotton, artichoke, stone fruit A number of fourth- increase as more products are registered Fenpropathrin 34,525 4,012 Cotton, grape, generation pyrethroids for additional California crops, includ- strawberry, orange have been registered ing fruits and vegetables. In general, Lambda-cyhalothrin 58,381 22,642 Alfalfa, lettuce, rice, during the past 20 years, they are cost-competitive as a direct ` tomato the most commonly substitute for the OPs and in some cases Permethrin 385,403 46,267 Lettuce, celery, used being esfenvalerate are even less expensive. spinach, almond (Asana) and lambda- Toxicity. In addition to efficacy and Neonicotinoids cyhalothrin (Warrior or cost, pyrethroids present a lower risk to Acetamiprid 6,632 3,519 Cotton, lettuce, celery, Karate). Because they are workers and applicators, as indicated by pear more effective against oral and dermal LD50 data (table 3). LD50 Imidacloprid 224,730 41,924 Lettuce, grape, cotton, insects at lower dosages is the dose that kills 50% of test animals cole crops than the third-generation to which a product is administered and Thiamethoxam 11,091 2,826 Cotton, tomato, pyrethroids, these con- is expressed as milligrams per kilogram melon, pepper temporary pyrethroids of body weight. Pyrethroid toxicity to * Active ingredient. Source: DPR 2003. are generally applied at amphibians, mammals and birds is much lower rates (typi- relatively low compared to the OPs;

12 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 Perhaps the most immediate insect-control problem for California agriculture will not be finding a suitable replacement for the organophosphates, but rather to delay the onset of and manage pest resistance to the pyrethroids and neonicotinoids that are replacing them. however, most aquatic invertebrates and are generally not compatible with bio- ity, nithiazine was not made commer- fish are highly susceptible (Smith and logical control programs. They also tend cially available due to its photolability. Stratton 1986). Acute toxicity expressed to persist for longer periods in the envi- Efficacy and cost. The efficacy of as 96-hour LC50 values (the concentration ronment and can be especially disruptive the neonicotinoids both as persistent lethal to 50% of a group of organisms when used in perennial crops. Pyrethroid systemic treatments and as less- within 96 hours) for esfenvalerate to use has been associated with outbreaks persistent foliar sprays offers excep- juvenile fish was reported at 0.25 mi- of secondary pests such as spider mites tional flexibility that is similar to that of crograms per liter (µg/L)(Werner et al. in orchards both during the season in some OPs. For example, imidacloprid

2002), while the respective 96-hour LC50s which they are applied and possibly in is currently available for systemic, seed, of diazinon are as much as 1,000-fold subsequent seasons (Bentley et al. 1987). soil, chemigation (applied via the ir- higher (EXTOXNET 2003). Molluscs are This will lead to increased use of miti- rigation system) and foliar applications. relatively insensitive to both OPs and cides and other chemical pesticides in The systemic activity of neonicotinoids pyrethroids, but have been shown to order to control these outbreaks. enables their integration into California bioaccumulate these chemicals, thereby agriculture as a satisfactory alternative to Neonicotinoids more selective representing a potential hazard to higher the OPs for the control of sucking insects, trophic levels within the food chain. There are four neonicotinoid in- as well as some Coleoptera (beetles) Water quality. The off-site move- secticides (synthetic chemicals based and Diptera (flies). However, the neo- ment of pyrethroids, a concern with the on the structure of nicotine) cur- nicotinoids will not control some insect OPs in California surface waterways, is rently registered for agricultural use orders — such as the Lepidoptera — as generally believed to be minimal due to in California — acetamiprid (Assail), effectively as the OPs, preventing their their hydrophobic chemical properties imidacloprid (Admire or Provado), thia- direct substitution for OPs and pyre- and generally high soil-adsorption coef- cloprid (Calypso) and thiamethoxam throids in many cases. This charac- ficients, which indicate that they will (Platinum or Actara). Nitenpyram is teristic of neonicotinoids is good for bind to surfaces they come into contact registered in California for flea control resistance management in that growers with rather than run off. However, data in cats and dogs. Others are under de- must utilize other available chemistries has recently been collected that found velopment. for some species rather than relying permethrin, esfenvalerate, bifenthrin and Imidacloprid was introduced in 1991 solely on one insecticide class for con- lambda-cyhalothrin in 75%, 32%, 25% as the first commercially available neo- trolling all insect pests. One limitation and 12%, respectively, of sediment sam- nicotinoid and is by far the most widely is their cost, which tends to be much ples taken from surface-water bodies in used (table 2). Like all neonicotinoids, higher than either OPs or pyrethroids. California’s Central Valley (Weston et al. it is a remarkably potent neurotoxic Toxicity. Neonicotinoids share with the 2004). With increases in pyrethroid use insecticide, which acts as a nicotinic acetyl- pyrethroids a relatively low risk of dermal likely, this may prove to be problematic choline receptor agonist. The target- toxicity to mammals (table 3), and their in the future (see page 5). site selectivity of imidacloprid and oral LD50s make them suitable for use on Secondary pests. Beneficial insects other neonicotinoids is a major factor in fruit and vegetable crops. As their regis- and mites are an important component their favorable toxicological properties tered crop uses expand on California’s of integrated pest management (IPM) because they act at much lower con- “minor use” or “specialty” crops (gener- since they can reduce the need for in- centrations in insects than in mammals. ally those grown on 300,000 acres or less), secticides when present at sufficient Imidacloprid was developed from nithi- they will likely replace many OPs. Where densities. Pyrethroids have been shown azine, a heterocyclic nitromethylene that they have already been registered, such as to seriously affect beneficial arthropods was first reported in 1978. Although it on lettuce and cole crops, their use is well present in agricultural crops, and they exhibited considerable insecticidal activ- established (table 2). Jack Kelly Clark Kelly Jack

Left, xylem is placed in a pressure bomb and will later be tested in the winged sharpshooter, center. The insect carries the pathogen that causes UC Riverside laboratory for neonicotinoid insecticides that kill the glassy- Pierce’s disease, which has killed vines in the Temecula Valley, right.

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 13 Water quality. Neonicotinoids are more similar to OPs than pyrethroids in their potential to move through the soil and run off in surface water. The California Pollution Contamination Prevention Act of 1985 established a set of specific numerical values (SNV) for pesticides and required DPR to place ac- tive ingredients on a list of candidates as potential leachers if their water solubility value exceeds 3 parts per million (ppm) or if the soil adsorption coefficient is less than 1,900 cm3/g, and if one of three persistence parameters is exceeded. The three major neonicotinoids currently registered in California all exceed the SNVs and are on the list, suggesting that care is needed when using these products to protect water quality. Imidacloprid is soluble in water (5.14 g/l), has moderate binding affinity to Top: left, UC Riverside postgraduate researcher Jian Bi catalogues peppers for an efficacy study of various alternatives to organophosphate insecticides, including neonicotinoids, pyre- organic materials in soils (Koc = 262) and throids, insect growth regulators and organic products; right, Ballmer collects insects using a a relatively long half-life in soils (365 suction sampler. Bottom: left, an adult potato psyllid; right, psyllid damage to a red pepper. days). Acetamiprid is also water-soluble (2.95 g/l), has similar binding affinity and its intended target. The OPs bind to similarity in binding sites. However, to organic materials in soils (Koc = 260), and inhibit the activity of the synaptic cross-resistance between insecticide but is short-lived in soils (1 to 8 days). enzyme acetylcholinesterase (AChE), classes having different modes of action Thiamethoxam is water-soluble (3.26 resulting in the disruption of the normal is viewed as a more serious problem, g/l), but has low binding affinity to transmission of nerve impulses across because insecticides to which an insect organic materials in soil (Koc = 43 to 77) the synapse. In resistant insects, insensi- has previously been unexposed may be and is more persistent (385 to 408 days) tivity of the AChE to binding by the OP jeopardized through the selective forces than the others. Soil type and irrigation restores synaptic function even in the of an unrelated insecticide. This can have practices will therefore be important presence of the OP. a serious impact on the development of considerations for growers in order to Pyrethroids bind to sites on the so- pest management strategies, particularly optimize neonicotinoid efficacy while dium channel and in so doing disrupt when emergency registrations of new preventing possible unwanted environ- the transmission of impulses along the insecticides are under consideration as mental effects. nerve axon by holding the channels in potential control agents. Detoxification Nontarget organisms. The impacts an open position (Bradbury and Coats mechanisms are an extremely impor- of neonicotinoids on nontarget organ- 1989). Pyrethroid resistance occurs tant source of cross-resistance between isms remain unclear. For example, there when mutations in sodium channel insecticides that differ in their target is some controversy over the safety of genes reduce the capacity of the py- sites. There are three broad groups of systemic treatments to both natural rethroids to bind effectively, thereby detoxification enzymes — the carboxy- enemies and bees that may encounter neo- enabling the channels to function nor- TABLE 3. Oral and dermal toxicities of commonly nicotinoid residues in nectar and pollen mally. Currently, there is no evidence for applied insecticides on California crops* (Schmuck et al. 2001). This is a current area target-site resistance in neonicotinoids. of research to better define specific risks and This is important because target-site Oral LD50 Dermal LD50 evaluate mitigation measures if necessary. resistance can act as a foundation upon Chemical name rat; mg/kg rabbit; mg/kg which other resistance mechanisms Organophosphates Pest resistance is a major concern develop. These in turn can disrupt Chlorpyrifos 96–270 2,000 Diazinon 1,250 2,020 The effective deployment of new management programs due to cross- Dimethoate 235 400 insecticides within pest management resistance to other insecticide classes. Pyrethroids programs should include strategies for Cross-resistance occurs in an insect Esfenvalerate 458 > 2,000 delaying the development of pest resis- when a resistance mechanism selected Lambda-cyhalothrin 1,593 > 2,000 tance. The two most common mecha- for in response to exposure to one Permethrin 430–4,000 > 2,000 nisms conferring resistance to the OP insecticide also confers resistance to Neonicotinoids and pyrethroid insecticides are target- a second insecticide to which the in- Acetamiprid 1,064 > 2,000 Imidacloprid > 4,870 > 2,000 site insensitivity and detoxification. sect has not been exposed. Target-site Thiamethoxam > 5,000 > 2,000 Target-site insensitivity arises from a cross-resistance is very common within * Higher LD50 values indicate lower oral or dermal toxicity. reduced binding between the insecticide individual insecticide classes due to the

14 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 Photos: Jack Kelly Clark Kelly Jack Photos: References Armegaud C, Labin M, Gauthier M. 2002. Effects of imidacloprid on the neural pro- cesses of memory in honey bees. In: Devillers J, Pham-Delegue MH (eds.). Honey Bees: Esti- Left, pyrethroids can be disruptive of natural enemies, such a the western orchard predator mating the Environmental Impact of Chemi- mite. Right, whiteflies are often the target of neonicotinoid applications. cals. London: Taylor Francis. p 85–100. Bentley WJ, Zalom FG, Barnett WW, Sanderson JP. 1987. Population densities of lesterases, the cytochrome P450s and the ber of pesticide applications (Ellsworth Tetranychus spp. (Acari: Tetranychidae) after glutathione-S-transferases — and each 1998) and the restoration of susceptibility treatment with insecticides for Amyelois of these has been implicated in resis- to synergized pyrethroids and nonpyre- transitella (Lepidoptera: Pyralidae). J Econ tance to the OPs and pyrethroids. throids (Dennehy et al. 1997). Entomol 80:193–200. Bradbury SP, Coats JR. 1989. Comparative Unfortunately, resistance to pyre- Delaying the onset of resistance toxicology of pyrethroid insecticides. Rev En- throids has already been reported for a viron Contam Toxicol 108:133–77. number of insect species in California The ultimate impact to California Byrne FJ, Castle S, Prabhaker N, Toscano NC. 2003. Biochemical study of resistance and elsewhere. The neonicotinoids, agriculture of losing OP insecticides will to imidacloprid in B biotype Bemisia tabaci however, are relatively new to Califor- depend very much upon how alterna- from Guatemala. Pest Manag Sci 59:347–52. nia agriculture, and there has yet to be a tive insecticides are deployed. Perhaps Dennehy TJ, Williams L, Russell JS, et substantiated case of resistance arising the most immediate insect-control prob- al. 1997. Monitoring and management of whitefly resistance to insecticides in Arizona. from their application under field condi- lem for California agriculture will not In: Dugger P, Richter E (eds.). Proc Beltwide tions. Continuous laboratory selection be finding a suitable replacement for the Cotton Conference; Memphis, TN. Memphis: of a whitefly population collected from OPs as insecticides, but rather to delay National Cotton Council. p 65–8. melon crops in the Imperial Valley re- [DPR] California Department of Pesticide the onset of and manage pest resistance Regulation. 2003. Summary of Pesticide Use sulted in 80-fold resistance to imidaclo- to the pyrethroids and neonicotinoids Report Data 2002 Indexed by Chemical. Sac- prid, illustrating that resistance genes that are replacing them. ramento, CA. http://www.cdpr.ca.gov. 500 p. are present in California whiteflies. The pyrethroids have an established Ellsworth PC. 1998. Whitefly manage- ment in Arizona: Looking at whole systems. Resistance has been documented in field history of use in California and much In: Dugger P, Richter E (eds.). Proc Beltwide populations of the silverleaf whitefly is known about their efficacy as pest Cotton Conference; Memphis, TN. Memphis: (Bemisia) in Arizona and worldwide in control agents, as well as their negative National Cotton Council. p 743–8. Spain, Israel and Guatemala (Byrne et impacts on nontarget species and the [EXTOXNET] Extension Toxicology Net- work. 2003. Pesticide Information Profiles. al. 2003). In the northeastern United environment. They are prone to resis- Oregon State University, Corvallis, OR. http:// States, resistance to imidacloprid was tance, and a concern is that they may ace.orst.edu/info/extoxnet/ detected in the Colorado potato beetle face additional problems with resistance Metcalfe M, McWilliams B, Hueth B, et al. 2002. The Economic Impact of Organophos- (Leptinotarsa decemlineata) just 2 years af- without their OP synergists. By contrast, phates in California Agriculture. California ter its initial use (Zhao et al. 2000). the neonicotinoids are a new class of Department of Food and Agriculture Report. The OPs are occasionally used in insecticide and their influence in pest Sacramento, CA. 41 p + app. www.cdfa. mixtures with pyrethroids to synergize control is only now being realized as ca.gov/publications.htm Roush RT, Tabashnik BE. 1990. Pesticide their activity. The synergistic effect is new products are developed and new Resistance in Arthropods. New York: Chap- believed to occur when the OPs inhibit uses identified. There is no evidence of man Hall. 303 p. pyrethroid-hydrolyzing esterases, there- resistance to neonicotinoids at present Schmuck R, Schoning R, Stork A, Schramel by enabling toxic doses of the pyrethroid O. 2001. Risk posed to honeybees (Apis mel- in California agriculture, although resis- lifera L, Hymenoptera) by an imidacloprid to accumulate at the target site. Mixtures tance has been documented elsewhere. seed dressing of sunflowers. Pest Manag Sci of the OP acephate (Orthene) and the It will be necessary for growers and 57:225–38. pyrethroid fenpropathrin (Danitol) were pest management specialists to use both Smith TM, Stratton GW. 1986. Effects of synthetic pyrethroid insecticides on nontar- used effectively for whitefly control on classes of materials judiciously and in get organisms. Residue Rev 97:93–120. cotton, although in recent years reliance combination with other alternatives as Werner IL, Deanovic A, Hinton DE, et al. on this strategy has suffered due to the feasible, to avoid resistance problems 2002. Toxicity of stormwater runoff after development of target-site resistance and maintain environmental quality. dormant spray application of diazinon and esfenvalerate (Asana) in a French prune to the pyrethroid, a mechanism that is orchard, Glenn County, California, USA. Bull not synergizable by the OP. In Arizona, Environ Contam Toxicol 68:29–36. a resistance management strategy was Weston DP, You JC, Lydy MJ. 2004. Distri- bution and toxicity of sediment-associated introduced in 1996 to combat whitefly F.G. Zalom is Entomologist, Agricultural Ex- pesticides in agriculture-dominated water resistance problems. A strategy of incor- periment Station, and Cooperative Extension bodies of California’s Central Valley. Environ porating insect growth regulators (IGRs), Entomologist, Department of Entomology, Sci Technol 38(10):2752–9. pyrethroids and nonpyrethroid conven- UC Davis; and N.C. Toscano is Cooperative Zhao JZ, Bishop BA, Grafius EJ. 2000. Inheritance and synergism of resistance to tional insecticides in a multistage pro- Extension Entomologist, and F.J. Byrne is imidacloprid in the Colorado potato beetle gram proved successful, as documented Assistant Research Entomologist, Depart- (Coleoptera: Chrysomelidae). J Econ Entomol by a dramatic reduction in the total num- ment of Entomology, UC Riverside. 93:1508–14.

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 15 REVIEW ARTICLE ▼ Pheromone mating disruption offers selective management options for key pests

Stephen C. Welter Carolyn Pickel Jocelyn Millar Frances Cave Robert A. Van Steenwyk John Dunley ▼

The direct management of insect pests using pheromones for mating disruption, or “attract and kill” ap- proaches, can provide excellent sup- pression of key lepidopteran pests in agriculture. Important successes to date include codling moth in pome Pheromones are used by insects (and numerous other species) to communicate. fruit, oriental fruit moth in peaches When these messages are disrupted, pest insects fail to reproduce and mate. A sprayable formulation of microencapsulated pheromone is applied by helicopter. and nectarines, tomato pinworm in vegetables, pink bollworm in cotton and omnivorous leafroller in vine- huge expanses of forests or plantations, However, the correction of the blend yards. Large-scale implementation to the regional disruption of mating eliminated the problem (Mochizuki et projects have yielded significant re- processes by pests, to smaller “attract al. 2002). and kill” approaches in specific fields. A key benefit of pheromone-based ductions in pesticide use while main- While many different groups of insects programs is that they are highly selec- taining acceptably low crop-damage use pheromones, most successes to date tive. Typically, only the primary target levels. Because of some difficulties have been with lepidopteran pests (but- species responds to the pheromone, and with high populations of pests, these terflies and moths); these successes have nontarget effects on biological control programs should not be viewed as allowed for more biologically intensive agents within a field or outside of a stand-alone strategies but rather as approaches to control pests. cropping system are not observed. The use of pheromones against key pests one tactic within a suite of integrated Advantages and disadvantages pest management options. does not result in outbreaks of second- Many advantages of pheromone- ary pests or pest resurgence, creating based pest management systems are opportunities for the biological control heromones, defined as chemicals common to other biologically based of other pest species. secreted externally by an organism management approaches, including However, the high degree of selectiv- toP send information to members of the virtually no detectable residues for ity may also be a significant obstacle same species, are used extensively by some dispensing systems, negligible to large-scale implementation, in cases insects to communicate with each other. health risks, a more rapid registration where secondary pests become a prob- Pheromones may signal information process and no accumulation in wildlife lem as insecticides are eliminated. as diverse as the sexual receptivity of or groundwater. Additional benefits Insecticide applications targeting the the producer, perceived dangers or the include reduced worker re-entry or pre- key pest sometimes inadvertently con- dominance of an individual in a colony. harvest intervals and limited impacts trol other pests as a collateral benefit. Researchers have interfered with these on other management practices, such as For example, outbreaks of leafrollers communication systems as a means to irrigation scheduling. Pheromone-based (such as Pandemis pyrusana) have been selectively control or manage pest spe- mating disruption has also been identi- reported in California apple orchards cies in agricultural and forest systems. fied as a strong tool for managing insec- utilizing pheromone-disruption pro- A variety of approaches employ ticide resistance. Whereas resistance to grams to control codling moth without pheromones to manipulate or disrupt pheromones applied over broad areas organophosphates (OPs)(Walker and the natural behaviors of insects, such might be expected, there is only one Welter 2001). Similar results were seen that population levels are reduced and documented case of resistance, when an in apple orchards under a variety of crop damage diminishes. These strate- incomplete pheromone blend was de- programs using the mating disruption gies include mass trapping efforts over ployed against the tea tortrix in Japan. of codling moth (Nicholas et al. 1999);

16 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 Pheromones may signal when the OP azinphos-methyl was re- vent moths from locating traps. Even in information as diverse as moved, populations of the wooly aphid conventional fields, pheromone traps the sexual receptivity of (Eriosoma lanigerum), lightbrown apple are rarely used as the sole indicator of moth (Epiphyaas postvittana), San Jose pest problems; rather, they are often the producer, perceived scale (Quadraspidiotus perniciosus) and used in combination with other ap- dangers or the dominance budworm (Helicoverpa spp.) increased. proaches, such as direct damage as- Other possible limitations include: (1) sessments. The use of high-dose lures of an individual in a colony. the lack of an identified pheromone for that still attract some moths even under Researchers have interfered some pest species; (2) high development mating disruption has proven useful with these communication and production costs; (3) requirements for tracking the flights of some pests for specialized application techniques or (such as codling moth) or as a supple- systems as a means to equipment; and (4) the need to supple- mental risk-assessment tool. Other spe- selectively control or ment the pheromone program in high cies, such as oriental fruit moth (Cydia pest-pressure situations. Pheromone molesta), do not exhibit this response. manage pest species. programs are most effective with low to However, it may be possible to develop moderate population densities, whereas nonpheromonal attractants for use in high-pressure situations in which dam- mating disruption (Light et al. 2001). logical factors behind these successes age from previous years exceeded 1% to appear to be the relatively long life and Approaches in the field 2% often require supplemental insecti- slow reproductive rate of the weevils, cide applications to prevent commercial Mass trapping is a direct control and the fact that the aggregation phero- damage. Treatment thresholds have strategy in which large numbers of mones attract both sexes. Success is been developed using modified phero- pests are captured and removed. This critically dependent on efficient mass- mone lures, but they vary between strategy has been successful in control- trapping to remove weevils faster than crops and regions. Mating disruption, ling large weevils in tropical crops such they can reproduce. like most other pest management strat- as oil palms, palmito palms (grown for In situations with other insects that egies, needs to be viewed within the hearts of palm), plantains and bananas. do not have these biological character- context of an entire pest management In oil palm plantations in Central and istics, and particularly with sex phero- system rather than as a stand-alone pro- South America, the palm weevil (Rhyn- mones that only attract one sex, mass gram. cophorus palmarum) is a vector of the trapping is generally less effective de- Monitoring the target pest with lethal red ring nematode. Pheromone- spite some larger projects collecting bil- pheromone traps also can become based mass trapping using one trap per lions of individuals (Ryan 2002). It has problematic, because the pheromones acre is now the principal control method been successful with smaller or confined used to disrupt mating will also pre- (Oehlschlager et al. 2002). The key bio- populations such as those found on islands (the sugarcane wireworm [Mela- notus okinawensis]) or with small, local- ized infestations of introduced pests

Jack Kelly Clark Kelly Jack targeted for eradication efforts, such as the white-spotted tussock moth (Orgyia thyellina) in New Zealand. Pheromone-based mating disrup- tion, which is the most commonly used approach, may work via a number of overlapping mechanisms that interfere with mate location and reproduction. Obviously, if males are prevented from locating or copulating with sufficient numbers of females, pest populations

Jack Kelly Clark Kelly Jack will decline. This approach works without the direct mortality of target individuals, preventing offspring and subsequent damage. Attracticides, or “lure and kill” strat- egies, combine an attractant with an insecticide, eliminating individuals that contact the lure. Many limitations of mass trapping also apply to programs By carefully monitoring crop damage and insect populations, and applying pheromones to disrupt mating, growers have successfully protected orchard crops from insect pests. that target males only. Depending on Left, former UC staff researcher Jeannine Lowrimore counts codling moths in a trap; how the system is implemented, it may top right, shoot-strike damage; bottom right, male peachtree borers in a pheromone trap. also interfere with the male’s location of

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 17 tion of mechanisms including camou- flage, competition between pheromone dispensers and females, habituation, and some advancement of the rhythm of the male’s response to the female’s pheromone, which may result in asyn- Pheromones can be applied using a variety of dispens- chrony in sexual behaviors. ers, including (clockwise The use of antagonistic compounds, from top left): microen- agonists, pheromone mimics and syner- capsulated pheromones, sprayed like insecticides; gists is broadly grouped under the term hand-applied dispensers, parapheromones, loosely defined as an- with a reservoir and perme- thropogenic compounds structurally re- able membrane to regulate lated to natural pheromone compounds release; hollow fibers; and twist-tie ropes. that affect the behavior or physiology

Jay Brunner/Wash. State Univ. Brunner/Wash. Jay of the insect’s communication system (Renou and Guerrero 2000). This group females through false trail-following, as nisms of mating disruption. Sensory includes compounds of plant origin well as the primary effect of the male’s adaptation is a reduction in the firing used to annihilate (with an attractant attraction to insecticide-laced baits. rates of the sensory structures after plus a lethal agent) the males of impor- prolonged exposure to the pheromone, tant dipteran pests, such as bait sprays Mechanisms of mating disruption whereas habituation is a reduction in for fruit flies or walnut husk flies. While Limitations to developing mating the insect’s response to the pheromone parapheromones alter neural activity, disruption programs include a lack of due to some change in the central ner- change insect behaviors and depress or understanding about the mechanisms of vous system. Both of these mechanisms synergize trap capture, their utility in mating disruption for different types of can generate the same nonresponsive the field for management purposes has dispensers, the biological or behavioral outcome. Different species respond received limited testing and remains characteristics of the target pest, and differently to prolonged exposures in highly variable. how pheromones move and distribute pheromone-treated fields. Habituation, However, studies have also shown themselves within agricultural systems which may result in arrested movement, that even in programs with minimal (Cardé and Minks 1995; Sanders 1997). has been proposed as a possible mecha- crop damage, significant mating may Surprisingly, the principle mechanisms nism for high-dose exposures from still occur. Alternative mechanisms are of action for even some of the most suc- devices that periodically release phero- being explored that focus on the effects cessful programs (such as codling moth mones in large aerosol puffs (puffers), of delaying mating rather than its com- in pome fruit) are unclear. or in close proximity to passive dispens- plete suppression. Delays in mating by Researchers have shown that the ers. Both can occur with either complete virgin females or males has been shown pheromone plume is not a uniform or partial pheromone blends. in multiple species to result in depressed cloud, but rather a series of filaments of The camouflage of a female’s phero- egg-laying and increased sterility of the pheromone interspersed with pockets mone plume presumes that the overlap- eggs laid (Jones and Aihara-Sasaki 2001; of zero to low concentrations due to ping plumes from multiple pheromone Fadamiro and Baker 1999). Therefore, natural turbulence in the air (Sanders dispensers generate a “fog” of phero- exclusive focus on the complete preven- 1997). The male is exposed to a series of mone, so that the males can no longer tion of mating may not be warranted. rapidly changing concentrations, which distinguish the pheromone emitted by Mating disruption still remains a useful requires both the interpretation of the a female from the elevated background. term if disruption is to include both the odor and a resetting of the antennal re- The false-trail-following mechanism prevention of mate location and mating, ceptors within milliseconds to perceive produces direct competition between and factors that interfere with or delay the next pheromone molecule (Leal calling females and synthetic dispens- the normal mating processes. 2003). The male proceeds to fly upwind ers, as males spend time and energy Pheromone-dispensing technologies in a series of surges interspersed with locating “false females.” This diversion crosswind casting when it detects pock- of the male’s activities results in either A variety of dispensing technolo- ets of air with reduced concentrations a decrease in the proportion of females gies have shown promise and success of pheromone. For most species, a tur- mated or a delay in mating. under commercial conditions and are bulent plume with pockets of high and The proposed mechanisms by which now available to growers. Each varies in low concentrations is required for prop- mating disruption might work are not terms of ease of application, cost and the er upwind flight; if a column of air is mutually exclusive, and several mecha- mechanism of disruption. Challenges for filled uniformly with pheromone, then nisms may be important for the same pheromone dispensers include protect- the sensory structures may fatigue and insect under different conditions. For ing components from degradation by no longer respond to the pheromone. example, Cardé et al. (1998) demon- environmental factors and the uniform Sanders (1997) and Cardé and Minks strated that the mating disruption of the release over time of different types of (1995) have reviewed different mecha- pink bollworm occurs from a combina- compounds (such as aldehydes, alco-

18 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 hols or acetates) with varying chemical and physical properties. MECs. Microencapsulated phero- mones (MECs) are small droplets of pheromone enclosed within a polymer capsule, which controls the pheromone release rate. The capsules are small enough to be applied as suspensions with the same commercial equipment used to spray insecticides. The effective field longevity of these materials gener- ally ranges from days to weeks depend- ing on climatic conditions, capsule size and properties, and the chemistry of the pheromone components. However, the material is applied directly to the com- Fig. 1. Downwind area of trap suppression by a single puffer with a 12-hour “on” cycle, modity, an important consideration in placed in a walnut orchard coincidental with the release of a uniform grid of sterile, food crops. marked codling moth. Number of moths is 5-day cumulative trap-catch total. Hand-applied dispensers. Larger, hand-applied dispensers include sys- of pheromone from the fiber, this tech- Current uses to control insects tems with an impermeable reservoir nology has a relatively constant emission fitted with a permeable membrane for rate over time. These fibers are often Pheromone-based devices have regulating pheromone release, and combined with an adhesive material dur- achieved the successful control of analogous laminate dispensers that con- ing application and may require special- insect pests in almost all types of agri- sist of a central pheromone-containing ized ground or air equipment to apply. culture, including perennial orchards, core sandwiched between two poly- High-emission dispensers. High- vineyards, annual vegetables and fiber mer films. These dispensers can be cut emission dispensers were developed crops. The following five insect pests into various shapes and sizes ranging to emit larger quantities of pheromone have enjoyed historical and recent suc- from larger, hand-applied dispensers and use fewer dispensers per acre to cut cesses with pheromone-based manage- to smaller, confetti-like flakes that can down on labor costs (Shorey and Gerber ment systems. be applied by specialized ground or air 1996; MafraNeto and Baker 1996). The Codling moth. A recent success in- applicators. Pheromones can be mixed only commercially available dispenser volves the management of codling moth into paraffin wax or aqueous paraffin of this type at this time is the Suttera in pear and apple orchards in California emulsions and applied directly to the puffer. The puffer uses a pressurized and the Pacific Northwest (Calkins and tree using hand-dispensers (Atterholt aerosol can filled with a pheromone, Faust 2003)(fig. 2). In 2001, the mating et al. 1999) or potentially in modified which dispenses metered puffs of pher- disruption of codling moth was used sprayers. omone at fixed time intervals (such as on about 135,000 acres of pome fruit, or Hand-applied dispensers also in- every 15 minutes). The number of units roughly 45% to 50% of the acreage from clude pheromone-impregnated poly- per acre varies depending on orchard the Sacramento Valley to the Pacific mer spirals, and twist-tie “ropes” that size and patterns of distribution, but ap- Northwest. Adoption rates in southern consist of a pheromone-filled plastic proximately one-half to one dispenser tube with a wire spline along one side. per acre is typical for codling moth in The wire allows these dispensers to be pears. twist-tied directly to the plant or hung Recent research attempting to de- indirectly with a clip. New technolo- fine the effective area of trap suppres- gies using alternative “rope dispensers” sion of codling moth, using uniform without a spline have been developed releases of sterile moths, revealed a as well. The larger reservoirs of the surprisingly long plume that was typi- hand-applied dispensers (ropes, lami- cally greater than 1,500 feet long and nate systems, spirals) allow for effective between 300 and 500 feet wide (fig. 1). lifetimes of 60 to 140 days, such that In addition, researchers are beginning single applications early in the season to test the possibility of using large, Fig. 2. Codling moth pheromone applications may suppress mating all season. passive-release devices consisting of in California in walnuts, apples and pears. To Hollow fibers. Hollow fibers have polymer bags loaded with large doses show use trends rather than absolute rates, been employed since the 1970s in mat- of pheromones (Mahr and Baker 2001). data includes all delivery technologies and ing disruption programs. The fibers These devices are intended to work in multiple applications to the same acre within a year. Sources: UC Integrated Pest Manage- consist of a short, impermeable plastic the same general way as puffers, but ment Web site, www.ipm.ucdavis.edu; Cali- tube that is sealed at one end and filled with no batteries or moving parts they fornia Department of Pesticide Regulation with pheromone. After an initial burst are potentially more reliable. pesticide-use tracking data.

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 19 Jack Kelly Clark Kelly Jack Jack Kelly Clark Kelly Jack

In Lake County, 15 pear growers uti- lized high-dose “puffer” dispensers on about 1,300 acres. The high-dose aerosol cans, inset, are hung high in trees, releasing the pheromones at regular intervals.

insecticide programs were failing because of extraordinary levels of re- sistance that jeopardized the whole industry by the late 1980s (Trumble 1997). Some damage suppression was achieved in cherry tomatoes, but dam- age levels were still variable and exces- sive in both conventional insecticide and pheromone-treated plots. A pest management program was developed to address resistance issues and pro- vide a more sustainable system, while considering its overall economics. For apple-growing regions are lower due to for codling moth was reduced 75%, winter and spring plantings, conven- higher pest population levels, presum- from an average of four to approxi- tional sites suffered excessive damage ably the result of more generations per mately one per season. of 75% to 90%, while damage was re- year. While the dominant release device This pattern was repeated with four duced to 33% to 35% in the IPM plots. from 1995 to 2000 was hand-applied additional areawide sites, initiated by Overall economic evaluations dem- dispensers (Isomate C+ rope dispensers a team of entomologists from UC, Or- onstrated substantial economic returns and Checkmate CM laminate dispens- egon State University, Washington State from the IPM program compared to ers), others such as puffers were suc- University and the U.S. Department conventionally treated plots. Phero- cessfully used on more than 1,300 acres of Agriculture’s Agricultural Research mone treatment remains relatively local of pears in Lake County. Service in Wapato, Wash. Ultimately, 17 and site-specific in California given that The use of mating disruption in additional sites were established in four tomato pinworm is a greater pest in pome fruit accelerated after the de- Western states. Although the areawide fresh-market than processing tomatoes. velopment of the first such areawide research programs are no longer ac- Newer products, including hand-applied program in the Randall Island region tive, the infrastructure and momentum or sprayable formulations, have been of the Sacramento River Delta in 1993. developed have allowed the approach introduced. However, the use of the Five growers and their pest control to flourish. Studies have shown that tomato pinworm mating-disruption advisors committed 760 contiguous codling moth also can be controlled in program was fairly flat from 1995 until acres to a long-term program to reduce walnuts with hand-applied dispens- 2000, when an increase occurred (fig. 4). codling moth populations over time, us- ers in smaller, more limited trials, but Pink bollworm. Pink bollworm ing a combination of mating disruption program costs were higher than con- (Pectinophora gossypiella) has been the and reduced insecticide. Codling moth ventional programs given the high costs target of an intensive, long-term and populations in an organic apple orchard of application to larger-canopied trees successful mating-disruption effort directly across the river plus additional (Grant et al. 2003). A similar result was (Staten et al. 1997) in both the United conventional sites were used for com- achieved in an areawide program in States and abroad. A variety of strate- parison. Lake County by Cooperative Extension, gies have been employed, including In the Randall Island project, popu- local pest control advisors and growers applications of hollow fibers, chopped lation levels in pheromone-treated using pheromone “puffers” on more laminate flakes, sprayable microencap- areas — as documented by mean trap than 1,300 acres owned by 15 growers. sulated pheromone, twist-tie ropes or counts — were reduced over the 6-year Tomato pinworm. The mating dis- laminate membrane dispensers. Prob- period to less than 10 moths per trap ruption of tomato pinworm (Keiferia lems with successful mating disruption from highs of about 80 moths per trap lycopersicella) was originally developed in fields with high moth populations (fig. 3). Fruit damage was held to less using hollow fibers in the 1970s and were detected and supplemental control than 1% in all years with final damage 1980s (Van Steenwyk and Oatman tactics were used. Combinations of ster- levels for 1998 to 1999 of less than 0.1%. 1983). It has been particularly suc- ile insects and mating disruption were The number of insecticide applications cessful in Mexico, where conventional implemented in large-scale programs in

20 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 the Imperial and Mexicali valleys. the introduction of Bt cotton, except in Successful mating disruption in areas under the pink bollworm eradica- the late 1980s in the Coachella Valley tion program that are not using trans- resulted in significant decreases in in- genic cotton. secticide use (7.3 applications in 1985 Oriental fruit moth. Mating dis- to no treatments in 1988). However, ruption has been used worldwide to the immigration of mated moths from control oriental fruit moth in stone the Imperial Valley to the Coachella fruit, peaches and nectarines using both Valley in 1989 appears to have resulted hand-applied and sprayable formula- in decreased program efficacy. The tions (Pickel et al. 2002). In 1995, a series isolation and areawide suppression of of replicated field plots was established Fig. 5. Oriental fruit moth pheromone appli- populations improved the efficacy of in California to evaluate three hand- cations in California peaches and nectarines. the mating disruption program, similar applied dispensers (laminate, mem- Data from DPR includes all delivery technolo- gies and multiple applications to the same to later experiences with codling moth. brane and rope dispenser) in peach acre within a year. Sources: see figure 2. A recent, interesting twist is the intro- orchards. Season-long control was duction of transgenic cotton with the achieved, with approximately 34% Bt gene, which has been reported as of the orchards having no detectable restricted. Sprayable formulations may highly effective against pink bollworm. damage and 63% having less than 3% be preferable to address more-local or Mating disruption has declined with damage, the current processor standard. less-severe infestations of omnivorous However, typically one orchard out of leafrollers, a pest that is unpredictable 21 in each year had damage in excess of in distribution and severity. 3%, which again reinforced that mating Future directions disruption in orchards with high moth populations needs to be supplemented While mating disruption provides with other control strategies. Overall an excellent management option for re- full-season costs for the pheromone pro- ducing insecticide use, it often requires gram were significantly higher than for supplemental insecticides to control conventional treatments, such that grow- high pest populations. The successful ers developed a modified program using implementation of mating disruption a single application of the hand-applied will require curative, rapid treatments pheromone dispensers supplemented to address increasing or unexpected with insecticides later in the season. The population surges. As outlined in partial pheromone program appears to Metcalfe et al. (2002), the implications be more cost effective at this time. of eliminating OP insecticides will More recently, both puffer-type dis- depend on the existence of alternative pensers and sprayable microencapsu- strategies, yet the implementation of Fig. 3. Codling moth (A) trap totals and (B) lated formulations have seen some use. pheromones may also require devel- damage levels for the season in pheromone- treated plots in the Randall Island project. Oriental fruit moth is an easily disrupt- opment of selective insecticides as ed pest, resulting in a large increase in supplements. applications from 1995 to 2000 (fig. 5). Programs are being developed to Increased adoption rates will depend address other lepidopteran pests in on growers’ perception of risk from systems for which the key insects may oriental fruit moth, the availability of be managed by pheromones or other se- effective, less expensive insecticide lective management tools. As key pests alternatives, and the complex of pests like codling moth come under control, within the orchard. research is under way to improve the Omnivorous leafroller. The mating mating disruption of other orchard disruption of omnivorous leafroller pests, such as the oblique-banded with hand-applied or sprayable formu- leafroller (Choristoneura rosaceana) and lations has increased since 1998 in Cali- Pandemis leafroller (Pandemis pyrusana). Fig. 4. Tomato pinworm pheromone use in fornia vineyards, with more than 35,000 Research is also ongoing in programs California for processing and fresh-market acre-applications made. Given that this that have had partial success, such tomatoes. Data from DPR includes all deliv- ery technologies and multiple applications pest is only important in the state’s as for navel orangeworm (Amyelois to the same acre within a year. Sources: see warmer grape-growing regions, the transitella). Opportunities with stored- figure 2. need for pheromones is geographically product pests such as the Indian meal

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 21 moth (Plodia interpunctella [Hubner]) or References Sacramento, CA. 41 p. + app. http://www. Angoumois grain moth (Sitotroga ce- cdfa.ca.gov/publications.htm Atterholt CA, Delwiche MJ, Rice RE, Millar JG, Daane KM, McElfresh JS, et realella) are being explored (Fadamiro Krochta JM. 1999. Controlled release of in- al. 2002. Development and optimization and Baker 2002). While most suc- sect sex pheromones from paraffin wax and of methods for using sex pheromone for cesses have been with lepidopteran emulsions. J Controlled Release 57:233–47. monitoring the mealybug Planococcus ficus insects, research in other insect orders Calkins CO, Faust RJ. 2003. Overview of (Homoptera: Pseudococcidae) in California areawide programs and the program for sup- vineyards. J Econ Entomol 95:706–14. — such as Heteroptera (e.g., stink pression of codling moth in the western USA Mochizuki F, Fukumoto T, Noguchi H, et bugs) or Coleoptera (beetles) — is directed by the United States Department of al. 2002. Resistance to a mating disruptant promising (McBrien et al. 2002; Millar Agriculture – Agric. Res. Service. Pest Manage composed of (Z)-11-tetradecenyl acetate in et al. 2002). Sci 9:601–4. the smaller tea tortrix, Adoxophyes honmai Cardé RT, Minks AK. 1995. Control of (Yasuda)(Lepidoptera: Tortricidae). Appl En- Some pests are highly mobile and moth pests by mating disruption – suc- tomol Zool 37:299–304. better suppressed at regional rather cesses and constraints. Annu Rev Entomol Nicholas AH, Thwaite WG, Spooner- than local scales. Coordinated area- 40:559–85. Hart RN. 1999. Arthropod abundance in an Cardé RT, Staten RT, Mafra-Neto A. 1998. Australian apple orchard under mating dis- wide efforts have been much more ef- Behaviour of pink bollworm males near high- ruption and supplementary insecticide treat- fective than patchworks of treated and dose, point sources of pheromone in field ments for codling moth, Cydia pomonella untreated areas. Newer formulations wind tunnels: Insights into mechanisms of (L.)(Lepidoptera: Tortricidae). Austral J Ento- such as puffers, attract-and-kill for- mating disruption. Entomol Experimentalis mol 38:23–9. Applicata 89:35–46. Oehlschlager AC, Chinchilla C, Castillo mulations and sprayable formulations Fadamiro HY, Baker TC. 1999. Reproduc- G, Gonzalez L. 2002. Control of red ring are offering opportunities to increase tive performance and longevity of female Eu- disease by mass trapping of Rhynchophorus program flexibility, mix strategies and ropean corn borer, Ostrinia nubilalis: Effects palmarum (Coleoptera: Curculionidae). Flor of multiple mating, delay in mating, and Entomol 85:507–13. reduce costs. adult feeding. J Insect Phys 45:385–92. Pickel C, Hasey J, Bentley W, et al. 2002. Perhaps the greatest challenges lie Fadamiro HY, Baker TC. 2002. Pheromone Pheromones control oriental fruit moth and with understanding the mechanisms puffs suppress mating by Plodia interpunc- peach twig borer in cling peaches. Cal Ag of mating disruption systems for dif- tella and Sitotroga cerealella in an infested 56:170–6. corn store. Entomologia Experimentalis Ap- Renou M, Guerrero A. 2000. Insect para- ferent target species and dispensers, plicata 102:239–51. pheromones in olfaction research and semio- which will allow the design of better Grant JA, Bentley W, Pickel C, Groh- chemical-based pest control strategies. Annu applications and protocols. Finally, the Lowrimore J. 2003. BIOS approach tested for Rev Entomol 45:605–30. implementation of mating disruption controlling walnut pests in San Joaquin Val- Ryan MF. 2002. Pheromones in Plant Pro- ley. Cal Ag 57:86–92. tection. Dordrecht: Kluwer Acad Publ. may require a shift in the scale at which Jones VP, Aihara-Sasaki M. 2001. Demo- p 256–78. growers, pest management consultants, graphic analysis of delayed mating in mating Sanders CJ. 1997. Mechanisms of mating extension specialists and university disruption: A case study with Cryptophelbia disruption in moths. In: Cardé RT, Minks AK illepida (Lepidoptera: Tortricidae). J Econ En- (ed.). Insect Pheromone Research: New Direc- researchers approach management tomol 94:785–92. tions. New York: Inter Thomson Pub. p 333–58. systems, given that overall program Leal WS. 2003. Proteins that make sense. Shorey HH, Gerber RG. 1996. Disruption performance is strongly correlated with In: Blomquist GJ, Vogt RG (eds.). Insect Phero- of pheromone communication through the large-scale, multigrower implementa- mone Biochemistry and Molecular Biology. use of puffers for control of beet armyworm Amsterdam: Elsevier Ac Pr. p 447–76. (Lepidoptera: Noctuidae) in tomatoes. Envi- tion efforts. Light DM, Knight AL, Henrick CA, et al. ron Entomol 25:1401–5. 2001. A pear-derived kairomone with phero- Staten RS, El-Lissy O, Antilla L. 1997. Suc- monal potency that attracts male and female cessful area-wide program to control pink codling moth, Cydia pomonella (L.). Natur- bollworm by mating disruption. In: Cardé RT, wissenschaften 88:333–8. Minks AK (ed.). Insect Pheromone Research: S.C. Welter is Professor and Chair of MafraNeto A, Baker TC. 1996. Timed, me- New Directions. New York: Inter Thomson Insect Biology, Department of Environ- tered sprays of pheromone disrupt mating Pub. p 383–97. mental Science, Policy, and Management, of Cadra cautella (Lepidoptera: Pyralidae). J Trumble JT. 1997. Integrating pheromones UC Berkeley; C. Pickel is IPM Advisor, Agric Entomol 13:149–68. into vegetable crop production. In: Cardé RT, Mahr D, Baker TC. 2001. Mating disrup- Minks AK (ed.). Insect Pheromone Research: UC Cooperative Extension, Sutter/Yuba tion for insect control: Where are we? In: New Directions. New York: Inter Thomson Counties; J. Millar is Professor, Department Proc 2001 Wisconsin Cranberry School. Univ Pub. p 379–410. of Entomology, UC Riverside; F. Cave is WI, Madison. p 1–4. Van Steenwyk RA, Oatman ER. 1983. McBrien HL, Millar JG, Rice RE, et al. 2002. Mating disruption of tomato pinworm (Lepi- Research Associate, and R.A.Van Steenwyk Sex attractant pheromone of the red- doptera, Gelechiidae) as measured by phero- is Cooperative Extension Entomologist, De- shouldered stink bug Thyanta pallidovirens: mone trap, foliage, and fruit infestation. J partment of Environmental Science, Policy, A pheromone blend with multiple redundant Econ Entomol 76:80–4. and Management, UC Berkeley; and J. components. J Chem Ecol 28:1797–818. Walker KR, Welter SC. 2001. Potential for Metcalfe M, McWilliams B, Hueth B, et al. outbreaks of leafrollers (Lepidoptera: Tortric- Dunley is Associate Professor, Department 2002. The Economic Impact of Organophos- idae) in California apple orchards using mat- of Entomology, Washington State Univer- phates in California Agriculture. California ing disruption for codling moth suppression. sity, Wenatchee, Wash. Department of Food and Agriculture Report. J Econ Entomol 94:373–80.

22 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 REVIEW ARTICLE ▼ Biological and cultural controls… Nonpesticide alternatives can suppress crop pests

Nicholas J. Mills Kent M. Daane ▼

Biological controls (the use of natural enemies) and cultural controls (the modification of cropping practices) provide valuable alternatives to or- ganophosphate insecticides (OPs) for Biological control has a long and rich history the suppression of major arthropod in California, beginning with the importa- crop pests in California. We discuss tion of the vedalia beetle for cottony cush- the successes and limitations of these ion scale in 1889. Above, some of the UC Sacramento Public Library/www.sacramentohistory.org Sacramento Room, pioneers of biological control and integrated two approaches with regard to tree pest management on an insect collection fruits and nuts, vines, and field and trip in Palm Canyon in 1948. From left to right: (top row) Huffaker, Fisher, Basinger; row crops. For example, a historic suc- (middle row) Bartlett, Hagen, Smith, Sellers, cess story is that the cottony cushion Huges, Compere, Steinhaus; (bottom row) Flanders, Finney, Fleschner, Timberlake, Di- scale remains innocuous in citrus pro- etrick, DeBach. Right, cottony cushion scale duction, more than 100 years after its was featured in a pest identification manual successful suppression by the vedalia for California published in 1888. beetle. More recently, growers’ use of groundcovers and road maintenance helps keep dust down on orchard roads to limit the buildup of web- complete their development); pathogens pests are unable to persist year-round spinning mites, and good vineyard (bacteria, fungi and viruses); parasites or to build populations quickly enough management is now synonymous (soil-inhabiting entomopathogenic nem- to suppress pest damage, their numbers with cultural controls for grape pests. atodes); and antagonists (less damaging can be augmented through the periodic Although such alternatives may not competitors). release of commercially produced natu- always be as effective and predictable Three broad categories describe how ral enemies. The inoculation of small as conventional insecticide programs, natural enemies are used in biologi- numbers of natural enemies can be used recognition that partial suppression cal control: classical biological control, to improve colonization at critical peri- augmentation and conservation. In ods for season-long pest suppression. can greatly reduce the need for OPs classical biological control, host-specific Likewise, the inundation of large num- will lead to the more widespread natural enemies are imported from the bers of natural enemies can be used for adoption of alternatives. exotic pest’s region of origin. On aver- immediate suppression, but often with- age, a new invasive pest has arrived in out a longer-lasting impact. iological and cultural controls can California every 2 months during the The third approach involves the con- provide alternative strategies to pest past decade (Dowell 2002) and, with servation of natural enemy populations managementB tactics that rely heavily on increasing global trade and travel, this of both exotic and indigenous pests broad-spectrum, neurotoxic insecticides, rate seems likely to continue or even through habitat manipulation or the particularly the organophosphates increase. In the best-case scenario, the alteration of crop production practices. (OPs). Biological control suppresses imported natural enemy will establish Natural enemies are often limited by pests via the action of their living and provide long-term suppression at the availability of essential resources natural enemies. Categories of natural low pest densities. A historic and stel- such as nectar or overwintering sites, enemies, in order of frequency of use in lar example is the 1889 importation to and the landscape within or surround- biological control, include: parasitoids California of the vedalia beetle from ing a crop can have a major impact on (parasitic wasps and flies that require Australia to control cottony cushion the effectiveness of biological control only a single host in which to complete scale, which was devastating the citrus among sites and regions. In addition, their development); predators (insects, industry. natural enemies often have a lower spiders and predatory mites that must In the second approach, when natural tolerance to many pesticides. As such, consume many prey individuals to enemies of either exotic or indigenous conservation tactics include habitat

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 23 The economic benefits of classical biological controls are evident from the multitude of historically important pests now held at low densities and all but forgotten. enhancements for natural enemies and and longtailed mealybugs — have long have occurred with indirect pests, such the use of selective pesticides. been suppressed through the action of as aphids, scales and whitefly, which do Cultural controls include the various imported parasitoids and predators. not damage the harvestable part of the means by which the crop can be made The olive scale, once a ubiquitous and crop; successes against direct pests, such less attractive, less available or less pal- destructive pest, is seldom encountered as fruit or nut borers, have been more atable to pests. The time frame for the in California olive groves due to the limited. However, all exotic pests are effectiveness of cultural controls can effective action of two complementary potential targets for classical biological range from a single harvest to the more parasitoids, Aphytis paramaculicornis and control, and even partial suppression can long-term suppression of pest activity. Coccophagoides utilis. Similarly, walnut significantly reduce the frequency and There are six key approaches to cul- aphid was considered the most impor- extent to which OPs need to be used. tural control, presented here in order of tant pest of walnuts before the importa- Augmentation. The most effective frequency of use. Sanitation is the remov- tion of the parasitoid Trioxys pallidus program involving periodic releases al of residual populations of pests from in 1969, and is now only an occasional of commercially produced natural en- crops, often during winter. Planting and problem when pesticides used against emies in tree fruit and nut crops is the harvesting dates can be altered to avoid other pests disrupt the parasitoid. use of the parasitoid Aphytis melinus coincidence with periods of high pest The great advantage of classical bio- for control of California red scale in activity. Crop rotation, particularly effec- logical control for tree fruits and nuts citrus (Collier and Van Steenwyk 2004). tive against soil pests, displaces crops on is that it can provide sustained control Approximately 5,200 parasitoids are an annual basis from pests with poor dis- of exotic pests without the need for fur- released per acre every 2 weeks from persal capabilities. Trap crops are used ther intervention. The perennial nature mid-February to mid-August to provide to attract colonizing pests into perimeter of these crops, and their low level of consistent reduction of red scale in the plantings where they can be readily de- seasonal disturbance for management San Joaquin Valley. Augmentation of stroyed by insecticide treatment or crop and harvesting, provides a more favor- A. melinus has been a commercially viable destruction. Diversification of the crops able environment for natural enemy program in citrus with costs comparable grown within and between fields can persistence and pest suppression. One to the use of OPs, but it can be rendered be used to reduce the attractiveness of a drawback is that not all invasive pests ineffective by disruption from broad- crop and the frequency of pest coloniza- of tree fruits and nuts have provided the spectrum pesticide sprays for thrips, soft tion. Nitrogen or irrigation levels can be same dramatic results. The best successes scales or glassy-winged sharpshooter. In manipulated to influence the susceptibil- this regard, for coastal citrus the parasit- ity of a crop to pest damage. oid Metaphycus helvolus has been released We discuss some of the successes in combination with A. melinus to provide and limitations of these biological and additional suppression of black scale. cultural practices in tree fruits and nuts, Among other tree fruit and nut crops, Photos: Larry L. Strand Larry L. Photos: vines, and field and row crops, as poten- experimental releases of the egg para- tial alternatives to OP insecticides. sitoid Trichogramma platneri for the sup- pression of codling moth in pears and Successes in tree fruits and nuts walnuts have shown that four weekly Classical biological control. There releases of 200,000 parasitized eggs per are numerous examples of successful acre each generation can reduce dam- biological control for the long-term sup- age by 60% for moderate populations of pression of exotic pests by imported codling moth (Mills et al. 2000). In addi- natural enemies in tree fruits and nuts. tion, releases of commercial predatory The cottony cushion scale remains in- mites (Galendromus helveolus and Neo- nocuous in citrus production, more than sieulus californicus) have proved effective 100 years after its successful suppres- against the persea mite in avocado. A sion by the vedalia beetle. Illustrating minimum of 2,000 predatory mites must how consistent this control has been, be released per tree when 50% of the flare-ups of cottony cushion scale oc- leaves have one or more motile stages of curred only after insect growth regula- the persea mite present (Hoddle 2002). tors applied to control California red Conservation. Although cover crop scale caused the disruption of vedalia management is considered important beetle pupation and egg hatch (Grafton- In many crop systems, the success of natu- for the conservation of natural enemies Cardwell and Gu 2003). ral enemies relies on the use of least-toxic in orchards, there is little clear evi- Other citrus pests — including or narrow-spectrum insecticides. Top, Walt dence that natural enemies active on Bentley of the UC Statewide Integrated California red scale and purple scale Pest Management Program investigates the orchard floor suppress pests in the in coastal areas, woolly and bayberry the use of mating disruption for the vine orchard canopy. In contrast, the use of whiteflies, and citrophilous, Comstock mealybug, bottom. selective pesticides to preserve naturally

24 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 occurring biological control has been none of which were A. epos, including Examples from vineyards the single most effective approach to the Anagrus commonly found in Califor- conservation biological control in tree Classical biological control. Despite nia vineyards (Triapitsyn 1998)! fruit and nuts. The majority of natural a 50-year history of research and devel- In the 1990s, a parasitic wasp, Pseu- enemies are negatively affected by OPs opment of biological control systems daphycus flavidulus, was imported to and other neurotoxic insecticides, so in California vineyards, there are few control obscure mealybug in Central switching to more selective products successful examples of imported natural Coast vineyards. Although it can be an can often lead to a substantial reduction enemies (Flaherty and Wilson 1999). effective natural enemy, the invasive Ar- in damage due to secondary pests (see However, the partial successes from gentine ant disrupts its potential impact. page 29). Without insecticide disruption, vineyards provide some important in- This example highlights the importance two-spotted and Pacific spider mites are sights for classical biological control. of effective competition from natural en- under effective natural control in most In the 1950s, the wasp Apanteles har- emies after release (Rosenheim and Wil- deciduous tree fruit and nuts through risinae and the parasitic fly Ametadoria hoit 1993). Currently, one of California’s the action of western predatory mites, misella were imported to suppress the larger biological control programs is other predaceous mites and predatory western grapeleaf skeletonizer. While being conducted for the glassy-winged beetles (Stethorus picipes). neither parasitoid effectively reduced sharpshooter, which vectors the bacteria Another example of effective natu- skeletonizer populations, nearly 40 that cause the devastating Pierce’s dis- rally occurring biological control is that years later, A. misella was shown to be ease. While egg parasitoids (Gonotocerus of citrus thrips in citrus orchards. The an important vector of a virulent granu- spp.) have been shown to kill more than predatory mite Euseius tularensis, togeth- lovirus, which is now part of effective 75% of the eggs deposited in the late er with other generalist predators, often biological control for skeletonizer. In the season, significantly reducing overwin- provide effective suppression of citrus 1980s, egg parasitoids, which were orig- tering populations, the level of control thrips — particularly in Valencia, but inally identified as Anagrus epos, were in vineyards may not be high enough also in navel oranges — unless disrupted imported from Arizona, New Mexico since economic injury levels are set to by insecticide sprays. Similarly, the use of and Mexico to control the variegated near zero tolerance. Often, biological pheromone mating disruption to replace grape leafhopper. A later taxonomic control agents do not provide the level OP sprays for codling moth management revision found that the imported para- of pest reduction needed when pests in apples and pears in the Western region sitoids were a complex of closely related vector plant diseases in vineyards. has led to substantial economic savings Anagrus species, each with slight dif- Augmentation. Predatory mites are on treatments for secondary pests due ferences in their geographic range, and released to control the Pacific spider to the enhanced activity of indigenous mite in San Joaquin Valley vineyards, natural enemies (see page 16). although release timing and rates have Cultural control. Sanitation is the been problematic (Flaherty and Wilson most important form of cultural control 1999). One possible improvement, and in tree fruit and nuts. Sanitation of over- an interesting concept in augmentation, wintered “mummy” nuts in the tree, is the combined release of predaceous by shaking or hand-poling, and on the mites along with less-damaging spe- ground, by disking or flail mowing, is of cies of phytophagous mites in order to particular importance for suppression supply predators with an early-season of navel orangeworm in almonds, pista- prey. Although the parasitoid Anagyrus chios and walnuts. In addition, harvest- pseudococci was imported for the classi- ing as soon as possible after hull-split cal biological control of vine mealybug, can significantly reduce nut damage. its impact is limited by ant activity and These two approaches, if used correctly, the short period during which mealy- can often provide effective control. bugs are found in exposed locations on Similarly, the removal of remaining and the vines. However, a combination of rat-tail fruit (small, thin fruit resulting least-toxic ant control, using sugar or from secondary bloom that hang onto protein baits, and inoculative releases the trees into late summer) after harvest of A. pseudococci timed to the movement has been shown to reduce overwinter- of mealybugs to exposed locations on ing codling moth populations in pears. the vine, has reduced mealybug damage Maintaining a groundcover and us- (Daane et al. 2003). ing water on roadways to reduce dusty Another example from integrated pest conditions in orchards can also be very Clark Kelly Jack management (IPM) in vineyards is the effective in reducing the buildup of Some biological control agents can eat oth- importance of matching the augmented web-spinning mites. In addition, the ers, often referred to as “intraguild preda- natural enemy to the targeted prey and tion.” Jay Rosenheim, top, UC Davis associ- avoidance of water stress can prevent ate professor of entomology, showed that release environment. Green lacewings high population densities, as water stress some predators such as the assassin bug, are released for leafhopper control, but leads to increased reproduction in mites. bottom, will feed on other predators. studies suggest that less than 30% pest

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 25 reduction has been achieved (Daane et bug sex pheromone (Millar et al. 2002). Field and row crop strategies al. 1993). There are three reasons for the Properly monitoring for this new, inva- poor success. First, while green lace- sive pest will reduce insecticide use. Classical biological control. In general, wings are considered generalist preda- Cultural control. Good vineyard examples of success in the classical bio- tors, leafhoppers are not a preferred host. management is now synonymous with logical control of exotic pests in field and Second, the release methods commonly cultural controls for vineyard pests. As row crops are less common than in other used for lacewing eggs result not only the season begins, basal leaves can be cropping systems, in part due to a lower in poor distribution, but also in high egg removed to improve the control of pow- incidence of exotic pests in these crops. mortality. Third, released lacewings are dery mildew, and this practice can also More importantly, the annual nature of often subject to a harsh environment, in- lower leafhopper densities. Throughout these crops, their greater level of seasonal cluding mortality from other predators. the season, dusty conditions and vine disturbance, and the highly dispersive Conservation. Cover crops have water stress are important components nature of many of the associated pests been popularly used to reduce vineyard of spider mite control, as mentioned are important barriers for the establish- pests such as leafhoppers. Still, the ben- for other crop systems. At the opposite ment and impact of introduced natural eficial role of cover crops with respect to extreme, too much irrigation water and enemies. For example, despite the estab- natural enemies is not clear. It is likely excessive vine vigor results in increased lishment of three parasitoids (Eretmocerus that cover crops have a dual role, chang- leafhopper densities (Daane et al. 1995). emiratus, E. mundus and Encarsia sophia) ing both the susceptibility of the vines For these reasons, maintaining balanced in California to combat the silverleaf to pests and the ability of the vineyard vine vigor — either through the use of whitefly, the highly migratory nature of to support natural enemies, leading to appropriate groundcovers, irrigation this pest and its ability to readily colonize a combined impact on pest densities and fertilization practices, or cultivar newly established fields has enabled it to (Costello and Daane 2003). selection — has become an essential escape effective parasitoid control. A classical example of conservation part of vineyard pest management. At In this regard, perennial field crops biological control from California vine- the end of the season, vines are cleaned such as alfalfa have the greatest potential yards is leafhopper control by Anagrus of unharvested grape clusters, and this for success in the introduction of natural egg parasitoids. Vineyard leafhoppers sanitation practice reduces omnivorous enemies for classical biological control. overwinter as adults, while Anagrus leafroller populations. In California, for example, both alfalfa parasitoids overwinter as larvae and aphids and weevils have been partially must find alternate leafhopper hosts controlled by introduced parasitoids for the winter, such as the blackberry (Summers 1998). Two different strains leafhopper or prune leafhopper (Fla- Phil Phillips (previously considered separate species) herty and Wilson 1999). Blackberry or of alfalfa weevils are present in Califor- prune refuges have been planted near nia: the western alfalfa weevil (confined vineyards in order to increase parasit- to cooler regions) and the Egyptian al- ism levels, but in practice these refuges falfa weevil (found in warmer regions). have not resulted in decreased leafhop- Initial releases of the larval parasitoid per densities because of the small size Bathyplectes curculionis in the 1930s re- of the refuge relative to the vineyard. duced western alfalfa weevil to almost A small blackberry or prune refuge undetectable levels in the mid-coastal will produce a correspondingly small region, but the parasitoid has not been number of blackberry or prune leafhop- effective in the warmer Central Valley pers. Anagrus densities reach a peak where the Egyptian strain predominates. in vineyards toward season’s end, and Release of a second strain of B. cur- these adult parasitoids will overwhelm culionis, probably originating from Iran, leafhoppers in the refuge. The result is extended control of western alfalfa wee- such a high percentage parasitism of vil to the mountain valleys in Northern Microctonus blackberry or prune leafhopper eggs Clark Kelly Jack California. Subsequently, that their populations are often elimi- aethiopoides, an adult parasitoid of the nated, thereby reducing the number Egyptian alfalfa weevil, has also been of overwintering Anagrus. The refuge established, although to date it has not works, but in the wrong direction! achieved the effective level of control The judicious use of selective pesti- seen in the northern and eastern United In classical biological control, natural enemies States. In addition, the control of spot- cides also conserves vineyard natural are imported from the pest’s native range, enemies. Even sulfur, which is approved identified and screened in quarantine. Top, ted alfalfa aphid in California has been for use in organic vineyards, can re- Serquei Triapitsyn, UC Riverside principal mu- achieved by the combined action of sult in increased spider mite densities seum scientist, has traveled through the na- three imported parasitoid species (Tri- tive range of the glassy-winged sharpshooter (Hanna et al. 1997). The most important to identify new egg parasitoids, such as Go- oxys complanatus, Praon exsoletum and recent advance in vineyard IPM is the notocerus ashmeadi, bottom, for the control Aphelinus asychis), together with the use identification and use of the vine mealy- of this invasive vineyard and citrus pest. of aphid-resistant cultivars.

26 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 Augmentation. Although lady maintain refuges for natural enemies plantings has proved valuable in restor- beetles, Trichogramma egg parasitoids (Summers 1998). The perennial nature ing limited adult food supplies for both and entomopathogenic nematodes have of alfalfa facilitates the maintenance and predators and parasitoids in a number all been used on occasion, there are few enhancement of natural enemy activ- of field crops, a good example being the examples of the successful use of com- ity, and the use of effective monitoring use of alyssum to encourage syrphids as mercially produced natural enemies in techniques to minimizing the need for aphid predators in Central Coast lettuce. field and row crops in California. This insecticide intervention is a key element Cultural control. Because most field is perhaps surprising, as the periodic of conservation biological control. and row crops are annual systems release of natural enemies has often With respect to annual crops, the requiring extensive manipulation for been considered the most suitable of the delays inherent in the colonization of planting and harvesting, cultural con- three approaches to biological control crops by natural enemies each season trols can readily be incorporated for in annual cropping systems (Obrycki et often allow early-colonizing pests to pest management. For example, sanita- al. 1997). Possible reasons for the lack escape natural enemy suppression. En- tion, planting and harvesting schedules, of success include the high cost of com- couraging early colonization to generate and variety selection are integral to the mercial natural enemy production, the predation pressure ahead of the normal effective suppression of silverleaf white- lack of data showing effectiveness and colonization of a crop by pests, a form of fly in cotton (UC IPM 2003b). Sanitation economic feasibility, and the misconcep- preemptive biological control, is intui- is used to remove crop residues and tion that mass-reared natural enemies tively appealing and has met with some weeds within and around the crop and can be used like insecticides. success (Summers 1998). Shelter strips prevent early whitefly colonization. It Trichogramma releases for the control within fields and perimeter plantings is also essential that vegetables, melons of fruitworms as part of an IPM pro- are known to encourage early natural- and alfalfa, which can generate substan- gram for insect pests in fresh-market to- enemy activity in field crops such as tial whitefly populations, be harvested matoes provides an illustrative example wheat, and the use of adult food sprays on as short a growing cycle as possible (Trumble and Alvarado-Rodriguez to attract green lacewing adults has pro- in cotton production areas. 1993). The releases of 247,000 T. pretio- vided promising preliminary results in Finally, the early termination of the sum per acre per week over a period cotton and sugar beet. In addition to the cotton crop itself, the use of smooth- of 5 to 9 weeks in multiple plantings encouragement of early colonization, the leaved Acala rather than Pima varieties, in Sinaloa, Mexico, reduced fruitworm use of nectar-bearing plants as perimeter and the prevention of regrowth after populations by 80% to 90%, and fruit harvest can also help to suppress white- damage was often comparable to plots fly populations. Although cotton is not treated with conventional insecticides. a favored host of Lygus bugs, migration However, despite the lower cost of David Rosen into cotton from surrounding weeds or Trichogramma production in Mexico and crops, particularly alfalfa, can also be a the substantial success shown by these problem. However, Lygus migrations pilot studies, Trichogramma releases have can be minimized through regional only been adopted by growers of pro- cooperation, staggering the harvest of cessing rather than fresh-market toma- alfalfa fields in an area, leaving alfalfa toes, and there has been no adoption of strips within harvested fields, or using this approach in California. Clearly crop trap crops, all of which ensure that suf- value, control costs, the predictability of ficient attractive alfalfa remains in the control and recognition of the value of area to reduce Lygus bug migration to partial success all play an important role nearby cotton. in the likelihood of adoption of augmen- Other field crops in which cultural tative biological control. controls have been of particular impor- Conservation. Dr. Ken Hagen was tance in California are alfalfa (Summers hired in 1951 as the first supervised con- 1998) and artichoke (UC IPM 2003a). trol entomologist in California to moni- Jack Kelly Clark Kelly Jack Effective alternatives for OPs tor pest-to-parasitoid ratios for alfalfa caterpillar, thereby taking advantage of Biological and cultural controls the control provided by an indigenous have proven to be effective alterna- natural enemy (Cotesia medicaginis) and tives to OPs for some major agricul- minimizing the need for insecticide tural pests. Classical biological control treatments. The importance of indig- The invasive Argentine ant, bottom (tending remains one of the best solutions for the enous predators and parasitoids as scale), disrupts biological control agents of control of newly invasive as well as long- natural controls for other alfalfa pests, aphids, scales and mealybugs. UC research- established exotic pests. The advantages including aphids and beet and western ers are developing programs that use small are clear — long-term pest suppression amounts of toxic insecticides mixed with sug- yellow-striped armyworm, has subse- ar bait to control ants in citrus and vineyards. without the need for toxic pesticides. quently led to the recommendation of Top, Phil Phillips, Ventura County IPM advisor, Once well established in a crop system, strip or border cuts for harvesting to tests a commercial liquid-bait station. however, effective natural enemies

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 27 are too often overlooked. Growers are more extensive monitoring of the crop Costello MJ, Daane KM. 2003. Spider and leafhopper (Erythroneura spp.) response naturally concerned with pests that are and often have a delayed action in the to vineyard ground cover. Environ Entomol currently causing crop damage, and suppression of pest damage. Finally, 32:1085–98. are often unaware of those pests that perhaps the most obvious intangible Daane KM, Sime KR, Cooper ML, Bat- are present in the crop system but held element is a grower’s personal decision tany MC. 2003. Ants in your vineyard? UC Plant Prot Quart 14(2):6–11. in check by the continued success of on how to best manage their land, and Daane KM, Williams LE, Yokota GY, introduced biological control agents. In protect and market their crop. Steffan SA. 1995. Leafhoppers prefer vines this manner, the importance and activity Can the practice of biological and with greater amounts of irrigation. Cal Ag of many introduced biological control cultural controls be increased? Their 49(3):28–32. Daane KM, Yokota GY, Rasmussen YD, et agents are poorly marketed in compari- impact and use vary among targeted al. 1993. Effectiveness of leafhopper con- son to insecticides that have a more pest species and crops. Their use is trol varies with lacewing release methods. visible treatment-and-effect relationship. dependent on numerous interrelated Cal Ag 47(6):19–23. Dowell RV. 2002. Exotic invaders and A recent example of the “invisible” components: effectiveness, cost, prac- biological control in California. Proc 3rd Cal action of an introduced biological con- ticality (how easily can they be used), Conf Biol Control. p 47–50. trol agent was provided by the flare- compatibility with other pest programs Flaherty DL, Wilson LT. 1999. Biological ups of cottony cushion scale caused and legislative restrictions on currently control of insects and mites on grapes. In: Bellows TS, Fisher TW (eds.). Handbook of by disruption of vedalia beetle activ- registered insecticides. The develop- Biological Control. San Diego: Academic Pr. ity following the use of insect growth ment and implementation of new bio- p 353–69. regulators for control of California red logical and cultural controls are driven Grafton-Cardwell EE, Gu P. 2003. Con- scale. Nonetheless, all successful clas- by need, which in itself often appears to serving vedalia beetle, Rodolia cardinalis (Mulsant)(Coleoptera: Coccinellidae), in sical biological controls will, eventu- be driven by the availability of effective citrus: A continuing challenge as new in- ally, be overlooked as alternatives to and environmentally safe pesticides. secticides gain registration. J Econ Entomol insecticides unless disruption occurs, Still, the application of biological or 96:1388–98. as the very attributes that result in pest cultural controls necessitates sufficient Hanna R, Zalom FG, Wilson LT, Leavitt GM. 1997. Sulfur can suppress mite preda- suppression also lead to the reduced background research and demonstra- tors in vineyards. Cal Ag 51(1):19–21. or even forgotten importance of the tions of efficacy, frequently requires Hoddle M. 2002. Persea mite biology target pest. Further, we suggest that the greater monitoring by pest control advi- and control. AvoResearch (Dec). 4 p. economic benefits of classical biological sors, and often faces a problem of com- Millar JG, Daane KM, McElfresh JS, et al. 2002. Development and optimization controls are evident from the multitude patibility between natural enemies and of methods for using sex pheromone for of historically important pests now pesticide use within a crop. In addition, monitoring the mealybug Planococcus ficus held at low densities and all but forgot- more widespread adoption of biologi- (Homoptera: Pseudococcidae) in California ten as key pests in the crop system. cal and cultural controls will require vineyards. J Econ Entomol 95:706–14. Mills N, Pickel C, Mansfield S, et al. 2000. Cultural controls can be effective greater investment in research, broader Trichogramma inundation: Integrating par- in reducing the susceptibility of all recognition of the importance of mul- asitism into management of codling moth. crops — but in particular field and tiple tactics and the value of partial sup- Cal Ag 54(6):22–5. Obrycki JJ, Lewis LC, Orr DB. 1997. row crops — to damage by indigenous pression, and the development of more Augmentative releases of entomophagous pests, and conservation and augmenta- selective insecticides that can be used species in annual cropping systems. Biol tive biological controls appear best suited when other tactics fail. Although the Control 10:30–6. for use in perennial crops. Cultural con- current new generation of insecticides Rosenheim JA, Wilhoit LR. 1993. Preda- tors that eat other predators disrupt cotton trols like augmentation and conservation shows low mammalian toxicity, in many aphid control. Cal Ag 47(5):7–9. require direct action and economic analy- cases they remain incompatible with Summers CG. 1998. Integrated pest sis by the farm manager. For this reason, natural enemies, suggesting that new management in forage alfalfa. Integr Pest their use is more often directly weighed priorities need to be incorporated into Manag Rev 3:127–54. Triapitsyn SV. 1998. Anagrus (Hyme- against the cost and effectiveness of in- the development of future products. noptera: Mymaridae) egg parasitoids of secticides. In our opinion, the adoption of Erythroneura spp. and other leafhoppers many biological and cultural controls then (Homoptera: Cicadellidae) in North Ameri- rests in managerial decisions based on in- can vineyards and orchards: A taxonomic review. Trans Amer Entomol Soc 124:77–112. tangible elements of the crop system. N.J. Mills is Professor, and K.M. Daane is Trumble JT, Alvarado-Rodriguez B. 1993. For example, crops marketed as or- Associate Specialist, Department of Envi- Development and economic evaluation of ganic have a limited range of chemical ronmental Science, Policy, and Manage- an IPM program for fresh market tomato controls available and, therefore, rely ment, UC Berkeley. They are Co-Directors, production in Mexico. Agric Ecosys Environ 43:267–84. more heavily on biological and cultural Center for Biological Control, College of [UC IPM] UC Statewide Integrated Pest controls for sustained pest manage- Natural Resources, UC Berkeley. Management Program. 2003a. Pest man- ment. In addition, farm size, time period agement guidelines for artichoke. www. ipm.ucdavis.edu/PMG/selectnewpest.arti- before harvest and potential for crop References choke.html damage will also influence decisions Collier T, Van Steenwyk RA. 2004. A criti- UC IPM. 2003b. Pest management guide- regarding the use of biological and cal evaluation of augmentative biological lines for cotton. www.ipm.ucdavis.edu/ cultural controls, which often require control. Biol Control 31:245–56. PMG/selectnewpest.cotton.html

28 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 REVIEW ARTICLE ▼ Various novel insecticides are less toxic to humans, more specific to key pests

Elizabeth E. Grafton-Cardwell Larry D. Godfrey William E. Chaney Walter J. Bentley ▼

A number of novel insecticides have recently been registered for insect control in agriculture. A major advan- tage of these new products is that they act on insect biological processes that humans do not experience, such as molting. Many also have greater selectivity to target specific species, so they are less likely to harm natural enemies when compared with the While often effective at controlling specific pests, less-toxic new insecticides can also have unintended impacts. When pyriproxyfen was broader spectrum organophosphate, sprayed to control red scale in citrus, it also caused gross abnormalities in carbamate, neonicotinoid and pyre- vedalia beetle pupae, left (normal) and right (abnormal). Vedalia beetles, inset (adult stage), are predators needed to control cottony cushion scale; throid insecticides. Such novel insec- as a result, secondary outbreaks of the scale occurred. ticides currently in use include four targeting lepidopteran pests, three targeting sucking insects, one specific selectivity and so are less likely to the novel insecticides have fairly short to dipteran leafminers and one insect harm natural enemies than the broad- residual activity or affect only immature spectrum organophosphate (OP), car- stages of insects, so the treatment timing growth regulator that controls a wide bamate, neonicotinoid and pyrethroid is less flexible compared with broad- range of insects. One negative aspect insecticides. As such, they are less likely spectrum insecticides. Finally, the cost of these insecticides is that because to cause outbreaks of secondary pests of the new insecticides is usually signifi- of their narrower range of activity — that are well controlled by natural en- cantly higher than the older products. controlling only a limited number of emies, and may be used as “clean-up” It is fortuitous that in recent years pests — growers may need to apply sprays to manage outbreaks of pests insecticides from different chemical additional pesticides for secondary caused by broad-spectrum insecticides. classes have been registered to control lepidopteran (primarily moths) and ho- pest groups that have poor biological The registration of these insecticides has helped to greatly reduce OP and carba- mopteran (primarily scales and white- control, increasing the total number mate insecticide use in California. This flies) pests, because many insects in of treatments per acre and total pest- has had an especially significant impact these groups have developed resistance control costs. in cotton, citrus and stone fruits, where to the older pesticides. The simultane- OP and carbamate use has been reduced ous registration of insecticides with number of novel insecticides with by as much as 70% since the late 1990s. unique modes of action allows growers unique modes of action were reg- The new insecticides also have some to alternate the insecticides used, reduc- isteredA during the late 1990s and early disadvantages. Because of their nar- ing the rate at which resistance devel- 2000s for insect control in agriculture. rower range of activity, each insecticide ops. Insecticide resistance in key pests These new insecticides have several generally controls only one pest group will continue to be a major impetus for advantages over older classes of insec- within a crop. The grower may need adopting novel insecticides. ticides. First, most of the products in to apply additional insecticides for Insecticides for Lepidoptera this group act on insect processes that secondary pests that have inadequate humans do not experience, such as natural control, increasing the total Four insecticides that have activ- molting. Low mammalian toxicity al- number of treatments per acre and total ity primarily affecting lepidopteran lows for short re-entry and preharvest pest-control costs. In addition, many of pests — indoxacarb (Avaunt, Steward), intervals, allowing the insecticides to Insecticide resistance in key pests will continue to be easily incorporated into pest con- trol programs. Many also have greater be a major impetus for adopting novel insecticides.

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 29 tebufenozide (Confirm), methoxyfeno- to each other, as well as spinosad and emphasizes the need for the rotation of zide (Intrepid) and emamectin benzoate Bt, helping to reduce the rate that insec- indoxacarb with emamectin benzoate, (Denim, Proclaim) — are registered for ticide resistance develops. the dibenzoylhydrazine insect growth a number of crops in California. The Indoxacarb. Indoxacarb is an oxadia- regulators (IGRs) and other insecticides greatest uses of these insecticides are zine insecticide that blocks the sodium to maintain the efficacy of all groups of in cotton, cole crops, lettuce, nuts, and channels in insect nerve cells, causing insecticides. stone and pome fruits (table 1). lepidopteran larvae to stop feeding Tebufenozide. Tebufenozide is a In stone fruit, the use of these insec- within 4 hours, become paralyzed and dibenzoylhydrazine stomach poison ticides — in combination with Bacillus die within 2 to 5 days (McCann et al. that acts as an IGR specifically for Lepi- thuringiensis (Bt) products, spinosad 2001). It is more effective as a stomach doptera. It mimics a molting hormone and mating disruption during the poison than as a contact poison. Indoxa- and blocks the completion of the nor- growing season — has greatly reduced carb is fairly selective, having activity mal molting process (Retnakaran et al. the need for dormant sprays of OP, car- primarily against lepidopteran larvae 2001). The insect stops feeding within a bamate and pyrethroid insecticides for and certain species of sucking insects few hours and undergoes a premature peach twig borer (Anarsia lineatella). This such as Lygus bugs. However, the activ- lethal molt within 3 to 7 days, becom- has benefited the stone fruit industry by ity of indoxacarb against the sucking ing trapped within the shedding head reducing pesticide residues in surface wa- insects is weaker than for Lepidoptera capsule. Tebufenozide must be ingested ter, by preserving natural enemies needed because of its slower bioactivation, to take effect and is thus slow-acting, for other pests such as San Jose scale lower sensitivity and a less favorable with a residual activity of 14 to 21 days. (Diaspidiotus perniciosus), and by reducing method of oral uptake in the sucking in- Application timing is critical, because secondary outbreaks of spider mite pests sects. Indoxacarb allows most predators it is more active on early larval stages caused by broad-spectrum-insecticide dis- and immature wasp parasites to survive (Waldstein and Reissig 2001). It is non- ruption of their natural enemies. (Hewa-Kapuge et al. 2003; Studebaker toxic to honeybees and is selective, not The Central Coast Vegetable Inte- and Kring 2003). However, the wet resi- affecting most natural enemies (Dhad- grated Pest Management Program for dues of indoxacarb are toxic to bees and ialla et al. 1998). pest management in lettuce provides adult wasp parasites. The crops for which tebufenozide is another example of the significant Indoxacarb controls important currently registered include cole crops, role that these narrow-spectrum in- pests in alfalfa, apples, cole crops, cot- cotton, grapes, lettuce, tomatoes and secticides play in Lepidoptera control. ton, lettuce and pears. Populations of some nuts, pome and stone fruits. Low Lettuce is highly susceptible to pest obliquebanded leafroller (Choristoneura levels of resistance to tebufenozide damage at the seedling stage and rosaceana) in Michigan (Ahmad et al. have been found in codling moth (Cydia during head formation. Many of the 2002) have exhibited resistance to in- pomonella), beet armyworm and oblique- seedling pests — such as crickets, flea doxacarb in regions where it has not banded leafroller populations that were beetles, aphids and whiteflies — are been used, suggesting cross-resistance not exposed to this insecticide (Moulton controlled with broad-spectrum OP, to older groups of insecticides. This et al. 2002; Ahmad et al. 2002), suggest- carbamate, pyrethroid or neonicotinoid insecticides. These insecticides reduce or eliminate the natural enemies that attack the lepidopteran pests, some- Clark Kelly Jack times causing outbreaks; selective in- secticides help to bring the Lepidoptera back under control without creating additional problems. In addition, there are a number of lepidopteran pests that attack both head and leaf lettuce, including cabbage looper (Trichoplusia ni), beet armyworm (Spodoptera exigua), corn earworm (He- licoverpa zea) and tobacco budworm (Heliothis virescens). Lepidopteran pests can destroy seedlings, bore holes and leave frass or insect body contaminants throughout the growth cycle of the let- tuce, necessitating multiple treatments. Because lettuce is highly susceptible to insect damage at the seedling stage, many Indoxacarb and tebufenozide provide growers spray broad-spectrum insecticides. Some newer, more selective insecticides unique, selective chemistries for these can bring lepidopteran pests under control without hurting their natural enemies and pests and act as rotational alternatives causing secondary pest outbreaks.

30 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 Omnivorous leafroller moth Peach twig borer larva attacking almond ing that there may be cross-resistance to Photos: Jack Kelly Clark Kelly Jack Photos: older classes of compounds, including OPs. There is also likely to be cross- resistance between tebufenozide and methoxyfenozide, because they have the same mode of action. These insecticides will need to be used infrequently, alter- nated with other insecticide chemistries, and coupled with alternative methods of control, such as mating disruption, to delay resistance in key pests. Methoxyfenozide. Methoxyfenozide TABLE 1. Novel insecticides primarily targeting Lepidoptera* is a dibenzoylhydrazine IGR, similar to tebufenozide in its mode of action, Indoxacarb its ability to induce a lethal molt and Crop Pests controlled its specificity for Lepidoptera (Carlson Alfalfa Egyptian alfalfa weevil (Hypera brunneipennis), various Lepidoptera et al. 2001). Methoxyfenozide was only Apple, pear Codling moth (Cydia pomonella) recently (2003) registered in California Cole Various cutworms, cabbage looper (Trichoplusia ni), and its use is likely to increase due to its diamondback moth (Plutella xylostella) better binding with lepidopteran recep- Cotton Cabbage looper, beet armyworm (Spodoptera exigua), tors and longer residuality compared western yellow-striped armyworm (Spodoptera praefica); with tebufenozide. Methoxyfenozide suppression of Lygus bug (Lygus hesperus) has a much lower ability to bind with Lettuce Corn earworm (Helicoverpa zea), tobacco budworm (Heliothis virescens), receptors in nonlepidopteran species, beet armyworm, various loopers making it a highly selective insecticide Stone fruit† Codling moth, oriental fruit moth (Grapholita molesta) and useful in a number of crops. Low levels of resistance to methoxyfenozide Tebufenozide in codling moth, beet armyworm and Crop Pests controlled obliquebanded leafroller have been Cole Cabbage looper, diamondback moth found, necessitating prevention precau- Cotton Alfalfa looper (Autographa californica), cabbage looper, tions similar to those for tebufenozide. saltmarsh caterpillar (Estigmene acrea), western yellow-striped armyworm Emamectin benzoate. Emamectin Grape Various leafrollers, skeletonizer (Harrisina brillians) benzoate is a second-generation aver- Lettuce Various loopers, beet armyworm mectin analog with exceptional activ- Stone fruit Codling moth, peach twig borer (Anarsia lineatella), oriental fruit moth, ity against lepidopterans, acting by omnivorous leafroller (Platynota stultana), decreasing the excitability of neurons. obliquebanded leafroller (Choristoneura rosaceana) Shortly after contact or feeding expo- Tomato Beet armyworm sure, the insect larvae stop feeding, be- Walnut, pistachio, Codling moth, obliquebanded leafroller, green fruitworms pear, apple (Orthosia hibisci, Amphipyra pyramidoides) come irreversibly paralyzed and die in 3 to 4 days. Emamectin benzoate toxic- ity is broader spectrum than methoxy- Methoxyfenozide Crop Pests controlled fenozide, tebufenozide or indoxacarb, Artichoke Artichoke plume moth (Platyptilia carduidactyla) which is a benefit in that it kills a wide variety of lepidopterans (Argentine et Cotton Beet armyworm, western yellow-striped armyworm; suppression of Heliothis species al. 2002). However, its broad-spectrum Grape Omnivorous leafroller, grape leaffolder (Desmia funeralis), activity also makes fresh residues toxic orange tortrix (Argyrotaenia citrana) to natural enemies (Studebaker and Nuts, stone fruit Navel orangeworm (Amyelois transitella), peach twig borer, oriental fruit moth, various leafrollers Kring 2003). Natural enemy survival improves after about 5 days due to Pome fruit Various leafrollers; codling moth suppression in conjunction with mating disruption Vegetables, cole Various armyworms, cabbage looper; suppression of diamondback moth rapid photodegradation. The toxic activ- ity lasts longer for the pest because the photodegradate moves through plant Emamectin benzoate Crop Pests controlled tissue (translaminar activity) and is toxic to the plant-feeding pest. Cole Cabbage looper, tobacco budworm, beet armyworm, various loopers Lettuce Corn earworm, tobacco budworm, beet armyworm, various loopers Emamectin benzoate is used primar- ily against pests in cole crops and let- * Current uses in California. tuce. (It is registered for cotton in other † Likely to be registered within a few years.

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 31 states, but not California.) Emamectin ate have shown only slight levels of re- pyriproxyfen is not fully compatible benzoate provides a rotational insecti- sistance (Waldstein and Reissig 2001). with natural enemies because it is high- cide for the control of caterpillars and so ly toxic to predatory coccinellid beetles, Treatments for sucking insects helps to reduce the development of re- halting both egg hatch and pupation sistance. Populations of obliquebanded Three insecticides — pyriproxyfen (Grafton-Cardwell and Gu 2003). The leafroller tested with emamectin benzo- (Esteem, Knack, Seize), buprofezin heavy use of pyriproxyfen in citrus for (Applaud, Courier) and pyme- California red scale control created a Silverleaf whitefly nymphs and pupae trozine (Fulfill) — have activity cottony cushion scale (Icerya purchasi) primarily affecting sucking in- problem due to the loss of vedalia beetle sect pests such as whiteflies and (Rodolia cardinalis). It may also be re- armored scales, many of which sponsible for pest resurgences in other Photos: Jack Kelly Clark Kelly Jack Photos: have developed resistance to OP, crops due to its effect on coccinellid carbamate or pyrethroid insecti- predators of armored scales, mealybugs cides. The greatest uses of these and mites. insecticides for whitefly control Second, pyriproxyfen has a narrower are in cotton and tomatoes, for range of activity compared with the car- California red scale (Aonidiella au- bamate and OP insecticides. Pyriproxy- rantii) in citrus, and for San Jose fen has no effect on the secondary pests scale in nuts, and stone and pome forktailed bush katydid (Scudderia fur- fruits (table 2). Their cost is often cata) or citricola scale (Coccus pseudom- significantly higher than OPs, agnoliarum), which lack natural enemies, carbamates and pyrethroids. and so these insects have become pri- Pyriproxyfen. Pyriproxyfen mary pests that must be controlled with is a pyridine compound that acts additional insecticide treatments. In as a juvenile hormone mimic past years, katydids and citricola scale IGR, inhibiting egg production were easily controlled by the OP treat- San Jose scale and the metamorphosis of im- ments applied for California red scale. mature stages into adults (Ishaa- Currently, pyriproxyfen is used in

TABLE 2. Novel insecticides targeting sucking insects* ya et al. 1994). It is most effective California to control pests in apples, in late-stage larvae or nymphs citrus, cotton, nuts, pears, and stone Foliar-applied pyriproxyfen and early pupal stages when and pome fruits. In bait form, it is effec- Crop Pests controlled juvenile hormone is normally tive against the protein-feeding native Apple Apple leafminer (Phyllonorycter species) low. It is active primarily against southern fire ant (Solenopsis xyloni). Citrus California red scale (Aonidiella aurantii) sucking insects such as scales, An extensive resistance-management Cotton Silverleaf whitefly (Bemisia argentifolii) pear psylla (Cacopsylla [Psylla] program has been developed for cotton pyricola) and whiteflies. It is also that limits the number of applications of Pear Pear psylla (Cacopsylla [Psylla] pyricola) effective against fire ants and pyriproxyfen to one per growing season Stone fruit, pome fruit, nuts San Jose scale (Diaspidotus perniciosus) apple leafminers (Phyllonorycter to reduce the rate of resistance devel- species). Because of its persis- opment. Caution should be exercised Buprofezin tence and efficacy, pyriproxyfen by growers as to the frequency of ap- Crop Pests controlled has been extremely effective in plication, because resistance has begun Almond San Jose scale, apple leafhopper reducing California red scale to develop in whitefly populations in Citrus California red scale and San Jose scale populations other areas of the world, even when the that developed resistance to OP number of applications per season was Cotton Silverleaf whitefly insecticides. It is safer for hy- limited to one (Horowitz et al. 2002). Grape Mealybugs (Pseudococcus species and Buprofezin. Planococcus ficus), leafhoppers menopterous parasites than OP Buprofezin is a thia- (Erthroneura elegantula and E. variabilis) insecticides, greatly increasing diazine IGR that disrupts molting by Stone fruit† San Jose scale parasite numbers and so improv- preventing chitin development (Uchida ing the control of both target et al. 1985). It is active primarily Pymetrozine and nontarget pests within crop against sucking insects such as scales, Crop Pests controlled systems. Pyriproxyfen is toxic whiteflies, mealybugs and leafhoppers, Cole, lettuce, Various aphids, various whiteflies to crustaceans, limiting its use although it also has activity against celery, tomato around bodies of water. beetles. Buprofezin is slow-acting Cotton Cotton aphid (Aphis gossypii) Citrus provides an example but persists a long time. It has poor

* Current uses in California. of two potential problems as- ovicidal activity, but treated adults † Likely to be registered within a few years. sociated with the use of IGR of some pest species may lay sterile insecticides in agriculture. First, eggs. It has little or no effect on lepi-

32 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 dopteran (moths), dipteran (flies) or hymenopteran (wasp) insects. Bupro- fezin is toxic to crustaceans, limiting its Clark Kelly Jack Photos: use around bodies of water. In citrus, buprofezin is not as ef- fective as pyriproxyfen in controlling California red scale because it requires Liriomyza leafminer adult Tunnels produced by leafminer larvae the majority of the scale population to TABLE 3. Current uses of cyromazine in California be in an immature stage (Grout and

Richards 1991). Buprofezin is less toxic Crop Pests controlled than OPs and carbamates to a number Cole, lettuce, pepper, spinach, Dipteran leafminers (Liriomyza species) of natural enemies, especially wasp celery, tomato, cucurbit parasites, allowing their numbers to greatly increase. However, similar to pyriproxyfen, it is highly toxic to coc- cinellid beetles, preventing larval molt- Pymetrozine is active against impor- tance to the older groups of insecticides ing (Grafton-Cardwell and Gu 2003). tant pests in cole crops, lettuce, celery around the world. Because leafminers Buprofezin use has led to outbreaks of and tomatoes. It has been registered for often require multiple insecticide treat- cottony cushion scale in citrus due to California cotton since 2001 to control ments, it will be important to rotate the loss of vedalia beetle. It also may cotton aphid (Aphis gossypii), but has not cyromazine with other insecticide be responsible for pest resurgences in yet been incorporated into management chemistries to combat resistance. other crops due to its effect on coccinel- programs to any extent. Pymetrozine A product with broad activity lid predators. must be applied when populations of Currently, buprofezin is used in cotton aphids are low, but in Califor- Diflubenzuron (Dimilin, Micromite) California to control pests in almonds, nia the treatment threshold for aphid is a benzoylphenylurea chitin-synthesis- citrus, cotton and grapes. Buprofezin populations has traditionally been fairly inhibitor IGR that disrupts molting. It has been an important component of high. When used for whitefly control, is slow-acting, requiring up to 14 days the silverleaf whitefly management pymetrozine causes adults to stop feed- for population reduction, because it is program for cotton, where it has helped ing, but it must be used in combination active against all molting stages. The delay resistance to insecticides. In with other insecticides such as IGRs to symptoms of diflubenzuron poisoning grapes, buprofezin can be rotated with reduce whitefly populations below the in grasshoppers include slowed move- the neonicotinoids to control mealybugs economic threshold. ment, uncoordinated jumping, loss of and leafhoppers and so help to man- legs, decreased feeding and malformed Controlling dipteran leafminers age resistance. Because of its selectiv- wings (Weiland et al. 2002). It is used ity favoring hymenopteran parasites, Cyromazine (Trigard) is a triazine against a variety of insects including buprofezin and parasites work together insecticide used as a chitin-synthesis- rice water weevils (Lissorhoptrus ory- to control grape and vine mealybugs. inhibitor IGR, which disrupts the molt- zophilus), beetles, various Lepidoptera, Buprofezin is likely to receive registra- ing of larval and pupal cuticles. It has grasshoppers, Mormon crickets (Ana- tion for San Jose scale in stone fruit in translaminar activity that quickly pen- brus simplex) and katydids. It does not the near future. etrates into leaves. It is active against cause mortality to adults, but does ster- Pymetrozine. Pymetrozine is a pyri- a very narrow range of insect pests, ilize the females of some species. dine azomethine. It is active primarily notably the larval stages of dipteran Because diflubenzuron is primar- against sucking insects such as aphids leafminers. Because of its high level ily active through ingestion, it is less and whiteflies. Its mode of action is not of specificity, cyromazine is much less toxic to a number of natural enemies, fully understood, but differs from other toxic to natural enemies, compared with especially wasp parasites. Similar insecticide groups. It interferes with IGRs such as diflubenzuron, making it to other IGRs, the eggs and imma- feeding behavior, resulting in the com- highly compatible with integrated pest ture stages of predatory beetles, as plete cessation of feeding within hours management (IPM) programs (Schuster well as lacewings, can be sensitive of contact (Harrewijn 1997). Aphids 1994). Cyromazine is nontoxic to crusta- to diflubenzuron (Ables et al. 1977). remain alive for 2 to 4 days before they ceans, bees, fish and birds. However, effects such as reduced egg die of starvation. Pymetrozine has The current uses of cyromazine are hatch can be rapidly reversed when been shown to reduce both direct dam- for Liriomyza leafminers in cole crops, the predators enter an untreated age and virus transmission by aphids lettuce, peppers, spinach, celery, toma- environment (Peleg 1983). Difluben- (Bedford et al. 1998). Because of its toes and cucurbits (table 3). Cyromazine zuron is toxic to crustaceans; however, specificity for sucking insects, it is rela- is important as a new chemistry for populations recover rapidly because it tively nontoxic to most natural enemies controlling dipteran leafminers, as a rapidly dissipates in water. (Sechser et al. 2002). number of species have developed resis- Currently, diflubenzuron is used to

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 33 Devastating Grasshopper.grasshopper

Harrewijn P. 1997. Pymetrozine, a fast-

Jack Kelly Clark Kelly Jack acting and selective inhibitor of aphid feed- ing. In-situ studies with electronic monitoring control pests in artichokes, citrus, cot- of feeding behavior. Pesticide Sci 49:130–40. ton, rice, nuts and stone fruits (table 4). Hewa-Kapuge S, McDougall S, Hoff- Diflubenzuron is also registered to man AA. 2003. Effects of methoxyfenozide, indoxacarb, and other insecticides on the treat grasslands infested with grass- beneficial egg parasitoid Trichograma nr. hoppers — which often devastate brassicae (Hymenoptera: Trichogrammatidae) nearby crops — providing an impor- under laboratory and field conditions. J Econ Entomol 96:1083–90. tant replacement for OP and carbamate TABLE 4. Current uses of diflubenzuron Horowitz AR, Kontsedalov S, Denholm I, in California insecticides. Resistance to diflubenzuron Ishaaya I. 2002. Dynamics of insecticide resis- in codling moth populations occurs in tance in Bemisia tabaci: A case study with the France (Sauphanor et al. 2000), indicat- Crop Pests controlled insect growth regulator pyriproxyfen. Pest ing the need for the careful rotation of Almond, stone fruit Peach twig borer Manage Sci 58:1096–100. Ishaaya I, De Cock A, Degheele D. 1994. this insecticide with insecticides that Artichoke Armyworms, artichoke Pyriproxyfen, a potent suppressor of egg have different modes of action. plume moth hatch and adult formation of the greenhouse Citrus Citrus leafminer whitefly (Homoptera: Aleyrodidae). J Econ Pros and cons (Phyllocnistis citrella), Entomol 87:1185–9. citrus peelminer McCann SF, Annis GD, Shapiro R, et al. Novel insecticide classes play a criti- (Marmara gulosa); 2001. The discovery of indoxacarb: Oxadi- cal role in the IPM of many California being tested for katydid azines as a new class of pyrazoline-type insec- crops. Excellent efficacy, high selectivity (Scudderia furcata) ticides. Pest Manage Sci 57:153–64. Moulton JK, Pepper DA, Jansson RK, Den- and low mammalian toxicity make them Cotton Beet armyworm nehy TJ. 2002. Pro-active management of attractive replacements for OPs and car- Grassland (near crops) Grasshopper, beet armyworm (Lepidoptera: Noctuidae) bamates, and the majority are considered Morman cricket resistance to tebufenozide and methoxyfe- nozide: Baseline monitoring, risk assessment, Rice Rice water weevil by the U.S. Environmental Protection and isolation of resistance. J Econ Entomol (Lissorhoptrus oryzophilus) Agency to be “reduced risk” insecticides. 95:414–24. However, their high level of selectivity Walnut Codling moth Peleg BA. 1983. Effect of 3 insect growth can increase the need for other insecti- regulators on larval development; fecundity and egg viability of the coccinelid Chilocorus cides if they allow secondary pests that bipustulatus [Col.: Coccinelidae]. Entomopha- lack effective natural enemies to gain References ga 28:117–21. primary pest status. In addition, the new Ables JR, Jones SL, Bee MJ. 1977. Effect Retnakaran A, Gelbic I, Sundaram M, et al. insecticides are not always completely of diflubenzuron on beneficial arthropods 2001. Mode of action of the ecdysone agonist associated with cotton. Southwest Entomol tebufenozide (RH-5992), and an exclusion selective, and the predatory beetles have 2:66–72. mechanism to explain resistance to it. Pest been especially sensitive to some of Ahmad M, Hollingworth RM, Wise JC. Manage Sci 57:951–7. them. Other problems include short re- 2002. Broad-spectrum insecticide resistance Sauphanor B, Brosse V, Bouvier JC, et al. in obliquebanded leafroller Choristoneura 2000. Monitoring resistance to diflubenzuron siduality and high cost. rosaceana (Lepidoptera: Tortricidae) from and deltamethrin in French codling moth Nonetheless, major impetuses for Michigan. Pest Manage Sci 58:834–8. populations (Cydia pomonella). Pest Manage the adoption of these chemistries in- Argentine JA, Jansson RK, Halliday WR, Sci 56:74–82. clude human health concerns and pest et al. 2002. Potency, spectrum and residual Schuster DJ. 1994. Life-stage specific toxic- activity of four new insecticides under ity of insecticides to parasitoids of Liriomyza resistance to OPs, carbamates and glasshouse conditions. Florida Entomol trifolii (Burgess)(Diptera: Agromyzidae). Int J pyrethroids. The wide variety of new 85:552–62. Pest Manage 40:191–4. modes of action is extremely helpful for Bedford ID, Kelly A, Banks GK, et al. 1998. Sechser B, Reber B, Bourgeois F. 2002. Py- The effect of pymetrozine, a feeding inhibi- metrozine: Selectivity spectrum to beneficial delaying resistance in key pests such as tor of Homoptera, in preventing transmission arthropods and fitness for integrated pest whiteflies, scales and aphids. As grow- of cauliflower mosaic caulimovirus by the management. J Pesticide Sci 75:72–7. ers and pest control advisors become aphid species Myzus persicae (Sulzer). Ann Studebaker GE, Kring TJ. 2003. Effects of familiar with the unique characteristics Appl Biol 132:453–62. insecticides on Orius insidiosus (Hemiptera: Carlson GR, Shadialla TS, Hunter R, et al. Anthocoridae), measured by field, green- of these insecticides, their adoption is 2001. The chemical and biological properties house and petri dish bioassays. Florida Ento- likely to increase. of methoxyfenozide, a new insecticidal ec- mol 86:179–85. dysteroid agonist. Pest Manage Sci 57:115–9. Uchida M, Asai T, Sugimoto T. 1985 Inhibi- Dhadialla TS, Carlson GR, Le DP. 1998. tion of cuticle deposition and chitin synthesis New insecticides with ecysteroidal and ju- by a new insect growth regulator, bupro- venile hormone activity. Ann Rev Entomol fezin, in Nilaparvata lugens. Stal Agric Biol E.E. Grafton-Cardwell is Extension and 43:545–69. Chem 49:1233–4. Research Entomologist, Department of Grafton-Cardwell EE, Gu P. 2003. Con- Waldstein DE, Reissig WH. 2001. Apple serving vedalia beetle, Rodolia cardinalis damage, pest phenology, and factors in- Entomology, UC Riverside; L.D. Godfrey is (Mulsant)(Coleoptera: Coccinellidae), in fluencing the efficacy of tebufenozide for Extension and Research Entomologist, De- citrus: A continuing challenge as new in- control of obliquebanded leafroller (Lepidop- partment of Entomology, UC Davis; W.E. secticides gain registration. J Econ Entomol tera: Tortricidae). J Econ Entomol 94:673–9. Chaney is Entomology Farm Advisor, UC 96:1388–98. Weiland RT, Judge FD, Pels T, Grosscurt Grout TG, Richards GI. 1991. Effect of bu- AC. 2002. A literature review and new obser- Cooperative Extension, Monterey County; profezin applications at different phenologi- vations on the use of diflubenzuron for con- and W.J. Bentley is IPM Entomologist, UC cal times on California red scale (Homoptera: trol of locusts and grasshoppers throughout Statewide IPM Program. Diaspididae). J Econ Entomol 84:1802–5. the world. J Orthoptera Res 11:43–54.

34 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 REVIEW ARTICLE ▼ Microorganisms and their byproducts, nematodes, oils and particle films have important agricultural uses

Larry D. Godfrey Elizabeth E. Grafton-Cardwell Harry K. Kaya William E. Chaney ▼

The insect and mite control potential of natural and biological toxins has been recognized for several centuries. Bacteria, viruses, protozoa and fungi are the primary groups of micro- organisms known to reduce insect populations; they often occur natu- rally in fields and function as compo- Natural and botanical products have been nents of biological control. Beneficial used to control insect pests for centuries. nematodes are also being used for Kaolin is a mineral-based particle film that is sprayed onto crops as a barrier to repel pest control, especially against soil in- insects and prevent feeding. sects. The isolation of toxic metabolic compounds from microorganisms con- tinues to be a fruitful research area, The insect-control potential of natu- biological agents that are being used although there are barriers to their ral and biological toxins has been rec- for pest control, especially against soil successful marketing and distribution. ognized for several centuries. As early insects. Several species of beneficial Another, more controversial way to as 2700 B.C., unintended epizootics nematodes are commercially available, (outbreaks of disease affecting many and the animal itself acts as a distribu- deliver these insect-specific toxins to animals of one species at the same time) tion tool for symbiotic bacteria that the target pest is through genetically by natural enemies (microorganisms) actually kill the target pest. As with the modified plants, such as those modi- were reported in beneficial insects such microorganisms, the ability to produce fied to express Bacillus thuringiensis as silkworms and honeybees. The first and formulate these nematodes into in- (Bt) toxins. Oils and particle films also record of microorganisms being inten- secticidal products has enabled their use have important niche uses for pest tionally used to control crop pests was in pest management programs. control. in the 18th century (a fungus against a A common feature of some micro- weevil pest). Bacteria, viruses, protozoa organisms, principally bacteria and and fungi are the primary groups of fungi, is their natural ability to produce pest management moves for- microorganisms known to reduce insect metabolic byproducts that are toxic to ward in the 21st century, alter- populations. These organisms often many organisms. For example, the nativeAS control measures are needed occur naturally in fields and function antibiotic penicillin was isolated from a to suppress insects and mites. Federal as a component of biological control. fungus and is used to combat bacterial regulators are closely scrutinizing the Research on these microorganisms as infections in humans. Other metabolic organophosphate (OP) and carbamate “biopesticides” has resulted in the abil- byproducts have toxic activity against insecticides under the Food Quality Pro- ity to isolate, culture and formulate arthropod pests. Instead of relying on tection Act (NRC 2000); in California, some for use in integrated pest manage- the microorganism to produce these surface-water contamination is of par- ment (IPM) programs. These formula- arthropod-active toxins in the field, ticular concern in the Sacramento and tions have improved the shelf life of the microorganism can be cultured in San Joaquin river water basins (USGS the resulting products, their miscibility fermentation facilities and the resulting 2000). The recognized adverse effects of with water or oil, and the ability to metabolites can be harvested, purified, synthetic chemical pesticides (such as spray them with commercial application formulated and used effectively against the OPs, chlorinated hydrocarbons and equipment, as well as provided some major arthropod pests. Two widely used carbamates) on the environment and protection against environmental ex- commercial insecticides, spinosad and human health emphasize the need to tremes that occur after application. abamectin, were developed using this advance and refine current pest- Entomopathogenic (insect-parasitic) approach. Over the centuries, as micro- management strategies (see page 7). nematodes are another example of organisms have evolved in their envi-

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 35 In most cases, the use of living organisms — with their inherent growth and survival criteria — introduces

considerable complexity into arthropod management schemes. Clark Kelly Jack Photos: ronment, the metabolites they produce following application, but also makes it have provided a competitive advantage; difficult to balance market size with reg- consequently, the isolation of these istration costs. In addition, microorgan- compounds continues to be a fruitful isms generally only have one mode of agricultural research area for the sup- entry into the host. Bacteria, viruses and pression of both arthropod pests and protozoa must be ingested to cause an plant pathogens. infection, whereas fungi cause an infec- One additional way of protecting a tion when the conidium (spore) attaches microbial-derived toxin and efficiently to and penetrates the insect cuticle. delivering it to the target pest is through Bt in widespread use genetically modified plants that express an insecticidal protein, such as Bacillus The notable exception, Bt, was used thuringiensis (Bt). Although there is con- on nearly 800,000 acres in California in siderable controversy worldwide regard- 2001 (DPR 2003). This bioinsecticide is ing the applicability and sustainability of registered on all California field, veg- this technology, it does undeniably rep- etable, orchard and floriculture crops. Bt resent an effective way to deliver a toxic strains (also known as subspecies) are ac- dose to the pest (Shelton et. al 2002). tive against particular groups of insects Other types of natural and biological (Tanada and Kaya 1993). These include toxins that are useful in pest manage- Bt kurstaki and Bt aizawai, which are both ment include plant-derived compounds active against lepidopterous larvae (but In the U.S. South, the cotton bollworm, top, is (such as rotenone, pyrethrum, sabadilla differ in which caterpillar species are controlled with cotton genetically engineered and azadiractin), inorganic products most susceptible); Bt tenebrionis, active to express Bacillus thuringiensis (Bt), but this (sulfur), mineral/refined petroleum oils against certain beetles; and Bt israelensis, pest is of minor importance in San Joaquin Valley cotton. Bottom, a cabbage looper killed and mineral-based particle films. active against mosquitoes and black flies. by a foliar application of Bt, the most widely Many of the alternative control Different Bt products are also char- used “bioinsecticide” in the state. agents that we discuss are not new to acterized by different insecticidal science. However, through innovative proteins, (δ-endotoxins) known as Cry approaches and with a better under- endotoxins A, B, C, and so on, and are and B. sphaericus, with efficacy against standing of how they kill insects and further subdivided into Cry1Aa, Cry Coleoptera (white grubs) and Diptera mites, many have come to the forefront 1Ab, Cry1Ac, and so on. These differ in (mosquitoes), respectively. Despite their in pest management. Others are still their toxicity to specific pests. Because commercial potential, these bacteria cur- plagued with high production costs, these products must be ingested, they rently have limited market share. inconsistent efficacy or special handling require warm weather for active feed- Nucleopolyhedroviruses. Nucleo- requirements, thereby limiting their ing and are most effective on early polyhedroviruses (NPV) can potentially usefulness in agricultural systems and instars. Crop damage may occur for a be used against lepidopterous larvae. as alternatives to broad-spectrum insec- short time, since Bt products are slow- A number of NPVs are registered in the ticides such as the OPs. acting, but the problems of slow kill and United States, with two of particular The natural epizootics of insect short residual activity are offset by their significance to California agriculture. pathogens occur commonly in native lack of toxicity to other natural enemies The NPV from the beet armyworm and managed systems, significantly (such as predators and insect parasites). (Spodoptera exigua) is registered in the assisting pest management. However, Bt products are especially important for United States with a provisional reg- except for Bt, the application of micro- pest control in organic cropping sys- istration for use in California in 2005 organisms for pest control in agricul- tems. However, some Bt products are (the California Department of Pesticide tural systems in California is extremely prohibited by some certifying agencies, Registration is requiring further data limited (Flint 1992). The reasons for this either because they contain inert ingre- with the actual product before full reg- include: (1) the high cost of in vitro or in dients that are prohibited, or because istration is granted), for use in field, vivo production; (2) limited persistence they have been genetically modified us- vegetable and floriculture crops. A simi- and efficacy due to UV light degrada- ing molecular techniques not acceptable lar product contains an NPV from corn tion, high humidity requirements or for organic production and marketing. earworm (Helicoverpa zea) and controls temperature sensitivity in the field; (3) this species and tobacco budworm (He- Activity of other microorganisms slow speed of kill; (4) poor shelf-life or liothis virescens); it has a provisional reg- special handling needs; and (5) high Active bacteria. Other bacterial spe- istration in California. Both viruses are levels of specificity. The latter can pre- cies have activity against insects, such as expected to get full registration for use serve populations of natural enemies Paenibacillus (formerly Bacillus) popilliae in California in 2005 or 2006.

36 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 Photos: Jack Kelly Clark Kelly Jack Photos:

Naturally occurring microorganisms, as shown above, can be isolated, Left to right, a cabbage looper killed by a nucleopolyhedroviris, and a rose cultured and formulated into commercial products for pest control. grass aphid and spirea aphid, both killed by fungal diseases.

Other microbial products that have et al. 1999). With fungi, considerable Genetically modified Bt plants been used commercially in the United research on pest control has been con- States or are registered with the U.S. En- ducted on Metarhizium anisopliae and Bt crops, genetically modified to vironmental Protection Agency (EPA) in- Beauvaria bassiana (the latter registered express the Bt toxin, have been widely clude a granulovirus (GV) of the codling as a commercial product) to control fo- used for pest control in many parts of the moth (Cydia pomonella), an NPV of the liage pests, but field uses are limited in United States as well as internationally. gypsy moth (Lymantria dispar), an NPV California, especially by the naturally Cotton and field corn are the most com- of the Douglas-fir tussock moth (Orgyia arid conditions present in many of the monly grown crops utilizing this tech- pseudotsugata) and a fungus (Lagenidium state’s agricultural production areas. nology in the United States (registrations giganteum) with activity on mosquitoes. Potential as replacements. At pres- are also in place on sweet corn and pota- Other microorganisms, such as the GV of ent, microorganisms appear to have toes), and thus far their efficacy against the Indian meal moth (Plodia interpunctel- limited potential for offsetting the loss target pests, primarily lepidopterous la) and a GV of the grapeleaf skeletonizer of OP and carbamate insecticides in larvae, has been exceptional. However, (Harrisina brillians), have generated some traditional agricultural production in genetically modified crops with efficacy interest but their market share may be California. Usage is limited, except for on other groups of arthropod pests, such too small for a commercial venture. the significant use of Bt. In most cases, as sucking insects or mites, have not Barriers to acceptance. Despite the use of living organisms — with their been marketed. The controversial aspects their effectiveness, several important inherent growth and survival criteria — of this technology include resistance factors have hindered the acceptance introduces considerable complexity into management, possible effects on nontar- of microorganism-based pest control arthropod management schemes. The get insects, the escape of modified genes products, as well as their limited com- selection of microorganisms adapted into wild plants or other cultivars, and mercialization and marketing. For for specific conditions where control is allergenicity and other health concerns in instance, the slow speed of kill of the needed — Central Valley cotton fields, humans. These issues, among others, are codling moth GV allows larvae to for example — may enhance their appli- beyond the scope of this article, but the inflict shallow wounds in apples, re- cability. In addition, the use of molecu- reader should be aware that the contro- ducing their marketability compared lar and classical genetics to improve the versy exists. with apples in synthetic-chemical pathogenicity of microorganisms may In terms of replacements for synthetic management programs (Kienzle et al. improve their performance as insecti- insecticides (OPs) in California, Bt crops 2002). There is a narrow window for cides. Classic research in this area has have had little impact through 2004. For the virus to infect codling moth larvae, been done at UC Davis, where the Au- crops available with the Bt technology in because once the larvae enter the fruit tographa californica NPV was engineered California’s Central Valley, lepidopter- they escape viral infection. Moreover, to encode an insect-selective neurotoxin ous pests are of minor importance or the GV has short persistence on foli- isolated from the venom of a scorpion are effectively managed by nonchemi- age and fruit (necessitating frequent (Androctonus australis)(McCutchen et al. cal means (such as cultural and phero- applications) and a narrow host range, 1991). This greatly enhanced the activity mone management strategies for pink which is an advantage for preserving and speed of kill of the NPV. However, bollworm [Pectinophora gossypiella] in natural enemies but a detriment in the public’s acceptance of genetic modi- cotton (see pages 16, 23). The unique terms of providing insecticidal con- fications to insect-pathogenic microor- environmental and cultural conditions trol of other arthropod pests (Cross ganisms is uncertain at this time. in California, compared with the rest of

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 37 Photos: Jack Kelly Clark Kelly Jack Photos:

Other commercially available pest-control products utilize natural chafer larva (left) and larva infected by the nemotode Heterorhabditis chemistries, functioning as components of pest control in agro- bacteriophora (right). Healthy spider mite adults, right, are killed by ecosystems. Left, the rice water weevil is infected by the fungus a microbial-based acaricidal product, abamectin, the metabolite of a Beauvaria bassiana (bottom). Center, healthy northern masked microorganism.

the United States, often result in a unique was isolated from a soil sample collected larvae). Spinosad is relatively fast- suite of arthropod pests. The crop diver- in Shizuoka Prefecture, Japan. Abam- acting — the insect usually dies 1 to 2 sity of minor-acreage crops in California ectin acts on insects by interfering with days after ingesting the active ingredi- has thus far limited the development neural and neuromuscular transmission ent and there appears to be no recovery. of Bt crops, as high volume sales are and paralyzes arthropods, resulting in Spinosad has excellent activity on needed to offset development costs. the cessation of feeding and death 3 to 4 lepidopterous larvae including the cot- days after exposure. Abamectin is most ton bollworm, peach twig borer (Anarsia Entomopathogenic nematodes effective when ingested by target ar- lineatella), armyworms (except western Two genera of nematodes, Steiner- thropods, but also works on contact. yellow-striped armyworm), loopers nema and Heterorhabditis, have been Abamectin penetrates leaf tissue and the saltmarsh caterpillar (Estigmene commercialized for pest control (Kop- and provides long-term (3 to 5 weeks) acrea). It also controls thrips. Registra- penhöfer and Kaya 2002). The nema- control of various mite species in field- tions are in place on almonds, stone todes are associated with bacteria in grown roses and other ornamentals, and pome fruits, citrus, cole crops and the genera Xenorhabdus for Steinernema strawberries, citrus, cotton and pears. A cotton. Spinosad is very short-lived, and Photorhabdus for Heterorhabditis. unique attribute of abamectin is that its sometimes necessitating additional ap- The nematode penetrates into the insect acaricidal properties are coupled with plications. A new formulation called host and releases bacteria that kill the activity on a few other insect species, Naturalyte was developed for the or- insect within 2 days. Unlike other insect especially dipterous and lepidopterous ganic crop industry. pathogens, nematodes are regulated by leafminers (Liriomyza and Gracillariidae, The organic mining of fermentation the U.S. Department of Agriculture’s respectively), the lepidopterous tomato products (byproducts from microorgan- Animal and Plant Health Inspection Ser- pinworm (Keiferia lycopersicella), citrus isms) could be a fruitful area for the vice (APHIS) and, therefore, are exempt thrips (Scirtothrips citri), fire ants in turf discovery of other compounds with from registration with the U.S. EPA. and the homopterous pear psylla (Caco- insecticidal properties in the future. These biological control agents psylla pyricola). As with synthetic insecti- The soil environment where actino- can be produced in vivo or in vitro, cides, the development of resistance is a mycete bacteria flourish is extremely formulated and applied like other soil concern; however, this has been largely complicated and diverse. For instance, pesticides. Because their natural habitat avoided to date, except in greenhouse milbemycins are structurally related to is the soil, they require moisture. They systems. With the exception of preda- the avermectins, and pesticidal products function best against insect pests in tory mites, abamectin is fairly nontoxic based on these byproducts are under cryptic habitats (such as soil-borne pests to natural enemies. development. More than 30 different and stem borers). Some use occurs in Spinosad. Spinosad (Success) was spinosyns have been isolated from greenhouses (for fungus gnats), land- fermented from the actinomycete bac- S. spinosa alone, and these are being scape crops and mushroom production terium (Saccharopolyspora spinosa). The evaluated for pesticidal properties. in California. Entomopathogenic nema- process yields several metabolites called Numerous other microbial species may todes have been proven effective against spinosyns, of which two biologically ac- also produce useful compounds. root weevils in citrus and scarab larvae tive compounds form the basis for the Natural toxins from plants in turf; however, in most cases syn- insecticide. The active ingredients are thetic insecticides are more widely used derived from a soil-dwelling bacterium Plant-derived compounds are an- against these pests in California. reportedly collected from an abandoned other fruitful area for the discovery of rum distillery on a Caribbean island in natural toxins for IPM. Botanical insec- Byproducts from microorganisms 1982. Spinosad kills susceptible species ticides are mainstays for pest control in Abamectin. Abamectin (Agri-mek, by causing the rapid excitation of the in- organic systems, but receive limited use Zephyr, Avid) is a microbial-based in- sect nervous system, leading to involun- in conventional systems. They are used secticide and acaricide (kills mites and tary muscle contractions, tremors and on vegetables, fruits and ornamentals. ticks) that is widely utilized and per- paralysis. Insects must ingest spinosad; Pyrethrum. Pyrethrum (as distinct forms like a conventional, synthetic in- therefore, it has little effect on sucking from synthetic pyrethroids) is the most secticide. This toxicant, produced by the insects and most nontarget predatory widely used plant-derived material, soil bacterium Streptomyces avermitilis, insects (it is highly toxic to syrphid fly with about 125,000 acres treated in Cali-

38 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 fornia in 2001. Pyrethrins are produced by certain species of chrysanthemums. Clark Kelly Jack The natural pyrethrins are contact poisons, which quickly penetrate the cuticle to the insect’s nervous system. A few minutes after exposure, insects are paralyzed. This quick knockdown is one of the strong attributes of pyrethrins.

However, enzymes in the insect swiftly Archives and Museum Collection Center Sacramento detoxify the natural pyrethrins and some pests will recover. To delay the en- zyme action so a lethal dose is assured, OPs, carbamates or synergists may be Above, in 1915 a worker sprayed dry sulphur added. The short residual activity of py- on young prune trees infected with brown rethrum on plant surfaces allows crops mite near Yuba City. Today, sulfur is still widely used as a pesticide to control mites on to be harvested shortly after application. grapes, citrus and other crops. Right, an air- Azadiractin. Azadiractin is extracted blast sprayer with tower treats citrus crops from seeds of the neem tree (Azadirachta with petroleum-based oils to control citrus indica). Chemically, azadiractin falls red mite and California red scale. within a class of compounds known as tetranortriterpenoids. The properties of applied as a baited toxicant for citrus Petroleum oils and particle films these insecticidal compounds include thrips and avocado thrips. Activity is feeding and ovipositional deterrence, affected by the percentage of alkaloids Petroleum-based oils have been used repellency, growth disruption, reduced in the extracted product and by the pH for a number of years to control insect fitness and sterility in a number of in- of the water used for the application. pests, especially mites and scale insects. sect species. The active ingredient is Because of sabadilla’s variability in Early formulations caused several prob- structurally similar to insect hormones activity for thrips control and its rapid lems because they had components that called ecdysones, which control meta- breakdown in light, spinosad and abam- were phytotoxic to plants. More recently, morphosis. Therefore, the disruption of ectin have largely replaced it in citrus petroleum oils have become highly re- the insect’s development and molting and avocado. However, when thrips fined and rarely show phytotoxic effects. process (interfering with their life cycle) develop resistance to spinosad and Their common distillation points are is likely to follow exposure. abamectin, as citrus thrips has to OPs, 415 and 440. The heavier 440 oils show Azadiractin is primarily used to con- carbamates and pyrethroids, interest in greater efficacy, but also more potential trol whiteflies, aphids, thrips, fungus sabadilla is likely to resume. for phytotoxicity. The 440 oils tend to be gnats, mealybugs, leafminers and other Other plants. Several other plants used in fruit and nut trees as dormant arthropods on food, greenhouse crops, produce compounds that are reportedly applications for mites and lepidopterous ornamentals and turf. Its acceptance toxic to arthropods. Cinnamaldehyde, and armored scale pests, often in combi- and usage in conventional agriculture derived from cinnamon oil, is the toxic nation with other pesticides. The lighter have been low, however, due to its er- element in the product Cinnamite. This 415 oils are used for in-season treatments ratic performance on major-crop insect product controls mites and aphids, as alone or in combination with other pes- pests. The more extensive use of this well as powdery mildew, on a range of ticides such as spinosad and abamectin. product in conventional agriculture is crops. Oils of rosemary, wintergreen, In citrus, 0.5% to 2% oil is used in spring limited by its narrow application win- clove, garlic and lemon are also sold and for citrus red mite (Panonychus citri) dow (during the susceptible life stage), reported to have insecticidal properties. and in the summer as a 1.4% spray for the need for frequent applications and a Certainly as insects and plants coevolved, California red scale (Aonidiella aurantii). narrow pest spectrum. plants developed defense compounds to Phytotoxicity can be avoided by treat- Rotenone. Rotenone is a nonspecific ward off attack by these herbivores. The ing during the coolest periods of the day insecticide with some acaricidal proper- isolation of these compounds could pro- and ensuring that the orchard is well ir- ties, which is used for pest control in vide useful crop-protection tools in the rigated prior to treatment. a variety of crops. It is extracted from future, but they are not cost effective in Presently, one product is available in several plants in the pea family. Because commercial agriculture today. the mineral-based particle film category. of its toxicity to aquatic animals, espe- Inorganic products. For arthropod Kaolin (Surround) is a naturally occur- cially fish, it should not be used near control, sulfur is the most commonly ring product, generally inert to mam- waterways. used inorganic product. Sulfur has mals, which does not react with other Sabadilla. Sabadilla is extracted from strong fungicidal properties and sec- materials (Glenn et al. 1999). When used seeds of the Mexican lily (Schoenocaulon ondarily controls spider mites. Sig- as a pesticide, kaolin is sprayed as a officinale), which contain the alkaloid nificant usage for spider mite control powdered suspension on crops, where veritrine as the active ingredient. It occurs annually on grapes, citrus, orna- it forms a barrier film that repels and is mixed with sugar or molasses and mental plants and cotton. prevents target pests from penetrating

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 39 Jack Kelly Clark Kelly Jack to be important niche products in Entomology Farm Advisor, UC Cooperative IPM systems. However, the util- Extension, Monterey County. ity of insect pathogens is limited by their specific requirements for References growth, survival and infectivity. Black CA, Karban R, Godfrey LD, et al. Certain toxic byproducts of 2003. Jasmonic acid: A vaccine against leafminers (Diptera: Agromyzidae) in celery. microorganisms are important Environ Entomol 32:1196–202. and robust tools for arthropod Cross JV, Solomon MG, Chandler D, et al. management today and may take 1999. Biocontrol of pests of apples and pears in northern and central Europe: 1. Microbial on an added role in the future. agents and nematodes. Biocontrol Sci Tech Research advances could over- 9:125–49. come the limitations of these con- [DPR] California Department of Pesticide trol agents and will likely Regulation. 2003. Summary of Pesticide Use Report Data 2002 Indexed by Chemical. Sa- discover and refine other types cramento, CA. http://www.cdpr.ca.gov. 500 p. of natural control strategies. Flint ML. 1992. Biological approaches to One such strategy is the area the management of arthropods. In: Beyond of “induced resistance,” whereby Pesticides: Biological Approaches to Pest Management in California. Oakland, CA. plants, once injured by an ar- DANR Pub 3354. p 2–30. thropod, are more resistant to Glenn DM, Puterka GJ, Vanderzwet T, et subsequent feeding and injury al. 1999. Hydrophobic particle films a new paradigm for suppression of arthropod (Karban and Baldwin 1997). This pests and plant diseases. J Econ Entomol 92: induction has been shown for 759–71. Certified organic growers often rely on plant- mite, thrips, aphid and leafminer Karban R, Baldwin IT. 1997. Induced Re- derived materials such as pyrethrum (extracted from injury in crops such as grapes, sponses to Herbivory. Chicago: Univ Chicago Pr. 319 p. chrysanthemums), azadiractin (from neem seeds), cotton and celery (Karban et al. rotenone (from several pea species), sabadilla (from Karban R, English-Loeb G, Hougen- Mexican lilly seeds), cinnamaldehyde (from cinna- 1997; Omer et al. 2001; Black et Eitzman D. 1997. Mite vaccinations for sus- mon oil) and other natural insecticides. al. 2003). The isolation of the tainable management of spider mites in vine- yards. Ecol Appl 7:183–93. compounds involved in this type Kienzle JC, Schulz C, Zebitz CPW, Huber the leaves or other parts of the plant. To of plant defense and the defining of the J. 2002. Persistence of the biological ef- be effective, the suspension must coat scope of the activity is ongoing. One fect of codling moth granulovirus in the all parts of the plants. Kaolin was regis- commercial product (Messenger) utilizes orchard — preliminary field trials. Proc 10th Int Conf Cultivation Technique and tered in California in 2000 for home use this technology through induction with Phytopathological Problems in Organic and commercial agriculture. Its target harpin proteins. Fruit-Growing and Viticulture, Feb 4–7, pests are widespread and include ear- Additional new natural pest-control 2002. Weinsberg, Ger. p 187–91. wigs, thrips, true bugs, aphids, hoppers, tactics, microorganism byproducts, Koppenhöfer AM, Kaya HK. Entomo- pathogenic nematodes and insect pest whiteflies, scales, beetles, caterpillars and and natural insecticides and acaricides management. In: Koul O, Dhaliwal GS (eds.). mites. Crop registrations include fruit, will likely be discovered to facilitate Microbial Biopesticides. London/New York: vegetable, and field and ornamental IPM programs. In conventional agricul- Taylor Francis. p 277–305. McCutchen BF, Choudary PV, Crenshaw R, crops. Kaolin has been used extensively ture, insecticides and acaricides from et al. 1991. Development of a recombinant in grape vineyards to repel glassy- microorganism byproducts are the baculovirus expressing an insect-selective winged sharpshooters (Homalodisca coag- “standards” for the control of certain neurotoxin: Potential for pest control. Bio/ ulata) from landing and transmitting the important arthropods, and some natural Technol 9:848–52. [NRC] National Research Council. 2000. bacterium Xylella fastidiosa, which causes products have important niche uses. The Future Role of Pesticides in U.S. Agricul- Pierce’s disease. However, kaolin caused These products are already important ture. Committee on the Future Role of Pes- outbreaks of California red scale in citrus tools against many pests in organic pro- ticides in U.S. Agriculture. Washington, DC: because it prevents natural enemies from Nat Ac Pr. 332 p. duction systems. Omer AD, Granett J, Karban R, Villa EM. gaining access to the scales. 2001. Chemically induced resistance against multiple pests in cotton. Int J Pest Man Contributions to IPM programs 47:49–54. Shelton AM, Zhao JZ, Roush RT. 2002. Insect pathogens, their insecticidal L.D. Godfrey is Extension and Research En- Economic, ecological, food safety, and social byproducts and natural insecticides and tomologist, Department of Entomology, UC consequences of the deployment of Bt trans- acaricides will make important contri- Davis; E.E. Grafton-Cardwell is Extension genic plants. Ann Rev Entomol 47:845–81. butions to IPM programs in a post-OP and Research Entomologist, Department of Tanada Y, Kaya HK. 1993. Insect Pathol- ogy. San Diego: Academic Pr. 666 p. era. These pathogens and natural toxins Entomology, UC Riverside; H.K. Kaya is [USGS] US Geological Survey. 2000. Water have been known for their pest control Professor, Departments of Nematology and quality in the Sacramento River Basin, Cali- properties for decades and will continue Entomology, UC Davis; and W.E. Chaney is fornia, 1994–98. USGS Cir 1215. 38 p.

40 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 RESEARCH ARTICLE ▼ Costs of 2001 methyl bromide rules estimated for California strawberry industry

Colin A. Carter James A. Chalfant Rachael E. Goodhue Gregory J. McKee ▼

The California Department of Pesticide Regulation (DPR) restricts pesticide use to reduce negative impacts on human health and the environment. The DPR implemented methyl bromide use regulations in 2001. Our study demonstrates that the estimated 2001 costs of these regulations for the California strawberry industry were quite substantial (more than $26 million total), equivalent to roughly Jack Kelly Clark Kelly Jack 25% of estimated industry returns Methyl bromide has been widely used in California — especially in strawberry production — to over total cash costs in 2001. These fumigate soil prior to planting and prevent nematodes and other soil-borne pests. The impacts were unevenly distributed California Department of Pesticide Regulation requires growers to warn the public of pos- sible exposure to the toxic fumigant. across growers. Growers with small fields in urban areas had higher per- the grower must obtain a permit from the United States and other developed acre costs than growers with large the county agricultural commissioner. nations in the 2005 calendar year (but fields in agricultural areas. Based on scientific assessments of the an exemption process allows critical potential effects of a pesticide on human uses to receive temporary waivers). The health and the environment, the DPR ban has been gradually phased in; the he California Department of Pesti- provides the commissioners with “sug- permissible quantity of methyl bromide cide Regulation’s (DPR) mandate gested permit conditions,” which reflect sold nationally is declining, and the rate isT to protect human health and the en- DPR’s judgment regarding “minimum of decline is linked to a percentage of vironment from the negative effects of measures necessary to protect people 1991 consumption. As of 2001 when we pesticide use (Federighi 2001). In order and the environment” (Federighi 2001). conducted our study, the main effect of to achieve this goal, the DPR uses a At their discretion, commissioners may the phase-out requirements on Califor- number of regulatory tools, including alter these conditions to reflect local cir- nia strawberry growers was a higher pesticide use restrictions. Use restric- cumstances. price for methyl bromide, whereas in tions are rules that are not included We examined the cost impact of use some other crops use had declined on the pesticide’s label, such as buffer regulations imposed in 2001 on methyl substantially. Overall, methyl bromide zones or application limits based on the bromide, a widely used preplanting soil usage in California strawberry produc- treatment date or location. Some use fumigant, on the California strawberry tion had not declined dramatically, and restrictions are intended to protect the industry. Human exposure to high con- remained at about 3.8 million pounds applicator’s health, such as protective centrations of methyl bromide can be in 2001 (table 1). Since 2001 the use of equipment requirements or limits on irritating to the eyes, airways and skin, methyl bromide in strawberry fields has the hours of exposure. Other use restric- while acute and chronic exposure can not substantially declined. tions are intended to protect other peo- lead to a degeneration of nerve cells. Strawberry growers fumigate the ple from exposure. Local environmental The regulations were aimed at reducing soil prior to planting in order to control impacts may be reduced by measures human exposure to methyl bromide by weeds, nematodes and other soil-borne such as prohibiting applications when limiting emissions and restricting hu- pests. While there are chemical alterna- the ambient air temperature is above a man activity near fumigation sites. tives to methyl bromide for strawberry specified threshold. Furthermore, under the United Na- production, their future availability is The DPR’s use regulations are ad- tion’s Montreal Protocol on Substances also in question due to human health ministered through a permit process. In That Deplete the Ozone Layer, methyl and environmental concerns. At the order to apply a restricted-use pesticide, bromide is scheduled to be banned in present time, one alternative fumigant,

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 41 TABLE 1. Methyl bromide (MBr) usage in California, 1996–2003

Total MBr Strawberry Calif. strawberry MBr applied applied in MBr applied share of MBr acreage per acre to Year California to strawberries usage using MBr strawberries* ...... lb...... % lb. 1996 16,022,069 4,383,611 27 21,345 205 1997 15,663,832 4,050,264 26 21,746 186 1998 13,569,875 4,257,364 31 20,291 210 Growers in areas with higher 1999 15,342,080 5,175,568 34 25,493 203 2000 10,862,836 4,234,905 39 22,580 188 population densities were much 2001 6,615,844 3,777,550 57 22,241 170 2002 6,594,515 3,706,589 56 20,501 181 more likely to be heavily affected 2003 7,562,718 3,671,982 49 20,593 178 by the buffer zone, permission and * Rate calculated using all MBr applied to strawberries, not only MBr reported on an acreage basis. Nonacreage use was less than 1% of strawberry use in 2002. notification requirements. Source: DPR 2003.

in 2001. In a typical year, strawberries 1,3-D, is on California’s Proposition 65 2001 fumigation regulations list of chemicals known to increase the rank as one of the top 10 most valuable risk of cancer, and is subject to township crops in the state (CDFA 2002). In 2001, The DPR methyl bromide use restric- caps; these limits are intended to regu- the leading counties in terms of value tions imposed in 2001 were complex. late lifetime exposure to 1,3-D. Another of strawberry production were Mon- Two types of buffer zones were specified: chemical alternative, chloropicrin, is terey (32.8%), Ventura (27.4%), Santa an inner buffer zone and an outer buffer currently being evaluated by the DPR Cruz (17.8%), Santa Barbara (9.0%) and zone. The size of each buffer zone de- under its risk assessment process. In Orange (6.2%), together representing pended on such factors as the size of the 2001, all chloropicrin products were put over 90% of the total value of produc- application block (acreage fumigated in into reevaluation by the DPR due to tion. Every year, growers expend almost a 24-hour period), the application rate, potential negative health effects at low $30,000 per acre to produce and harvest the method of application, the proximity doses (DPR 2004). strawberries, so even a 30-acre farm of the field to houses or other occupied The overall economic impacts of the has an outlay of about $1 million per buildings, and the willingness of neigh- global methyl bromide ban are also un- year. Based on the UC cost and return bors to allow the fumigation to proceed. clear. Analyses of the economic viability budgets for strawberries, statewide net For both types of buffer zones, the opera- of methyl bromide alternatives using field grower returns above total cash costs tor had to obtain permission from the trial results have had mixed results (Good- are roughly $103.7 million (Klonsky and neighboring landowner to extend the hue et al. in press). According to DPR’s De Moura 2001). buffer zone onto the adjacent property. pesticide use report, in 2002 roughly 25% of California’s strawberry acreage was fumigated using methyl bromide alternatives, which suggests that some

growers find them economically superior Clark Kelly Jack to methyl bromide (DPR 2003). It is dif- ficult to evaluate the contribution of the DPR use regulations to this shift. Our analysis focused on the impact of the 2001 methyl bromide use regu- lations on industry costs. We did not incorporate any changes in industry revenues that may offset these costs, nor did we measure the total social costs and benefits of the regulations. Estimating the human health and other benefits of the 2001 methyl bromide use regulations was beyond the scope of our analysis. Similarly, we did not attempt to measure the costs of the use regula- tions to anyone besides growers. California strawberry industry Due to its impact on the ozone layer, methyl bromide is being gradually phased out. Above, one California’s total fresh and processed alternative fumigant is a mixture of 1,3-dichloropropene and chloropicrin, which is injected into strawberry sales were $805.8 million the irrigation system. However, these chemicals are also subject to strict regulatory controls.

42 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 Shachar Shem-Tov/UC Davis Shachar Shem-Tov/UC Courtesy of Hussein Ajwa/UC Davis Ajwa/UC Courtesy of Hussein

In 2001, state regulators imposed new regulations on methyl bromide applications, which included buffer zones to limit exposure. The authors found that many strawberry growers were forced to switch from bed fumigation, left, where the beds are formed and then treated, to more expensive flat fumigation, right, in which the process is reversed.

The inner buffer zone extended a total acreage, holding other factors Impacts of regulations minimum of 50 feet from the edge of constant. For example, a square 10-acre the application block, and increased To evaluate the costs of the 2001 field with one 50-foot buffer extending with the size of the acreage block and DPR methyl bromide fumigation regu- into the field itself would not be able to the application rate. Only individu- lations for the California strawberry in- fumigate 7.6% of its total acreage. If it als involved in the fumigation process dustry, we collected copies of available, had two adjoining buffered sides, the were allowed into the inner buffer zone. completed fumigation permits and nonfumigated acreage would increase These individuals were subject to ad- worksite plans for strawberry fields in to 14% of the total; 21.6% and 28% of the ditional use restrictions, which specified the five counties producing the most total acreage would be nonfumigated the maximum exposure times for vari- strawberries: Monterey, Orange, Santa for three and four buffered sides, re- ous fumigation tasks. The inner buffer Barbara, Santa Cruz and Ventura. In to- spectively. Fields near urban areas were zone had to be on agricultural land or tal we collected more than 400 worksite more likely to be unable to fumigate a a public roadway and could not extend plans and permits for 2001 from the greater share of acreage than those in onto any adjacent nonagricultural land. county agricultural commissioners’ of- agricultural areas. The outer buffer zone extended at fices. Simulation analysis was conduct- For a given buffer-zone restriction, least 60 feet from the edge of the block ed using work-plan data to determine smaller fields lost a larger percentage and increased with the size of the acre- the effects of the buffer zones. This of their total acreage. For example, a age block and the application rate. Peo- involved the development of a math- square 20-acre field with one buffered ple were allowed into the outer buffer ematical model of the fumigation regu- side had 1.07 nonfumigated acres, or zone for transit purposes or to “conduct lations; we then asked the model to 5.4% of the total. In contrast, a square activities approved by the county agri- solve for optimal fumigation practices, 10-acre field had 0.76 nonfumigated cultural commissioner.” Here, individual given the many different field configu- acre, or 7.6% of the total. This differ- exposure was limited to no more than rations found in the work-plan data. ence increased with the number of 12 hours out of any 24. The outer buf- Our analysis also utilized information buffered sides. If all four sides were fer zone was not limited to agricultural from about 20 growers identified by bordered by nonagricultural uses, the land. Even if the buffer-zone require- the county agricultural commissioners’ 20-acre field’s nonfumigated acreage ments were not binding, the 2001 DPR offices and encountered at field days would be 20.3% of the total, while the regulations limited total acreage for a and other venues. 10-acre field’s nonfumigated acreage single fumigation block to a maximum Buffer zones. A notable impact of would be 28%. of 40 acres in any 24-hour period. the DPR regulations on growers was The difference in percentage of acre- A neighborhood notification require- that some acreage could no longer be age lost increased with the difference ment was also included in the use fumigated with methyl bromide due to in field size. For a square 50-acre field, restrictions. It specified that property the buffer-zone requirements. This im- 3.4% of its acreage would be nonfumi- owners within 300 feet of the outer pact varied by location, field size and gated when it had one buffered side, buffer zone had to be notified that an field shape. As a result, growers had and 13.1% would be nonfumigated application permit had been approved to replace the strawberries that would when it had four buffered sides. Aver- at least 9 days prior to the initiation of have been grown on this acreage with age field size by county varies: in the fumigation. Those receiving the initial a less valuable crop, or they suffered work plans we collected, it ranged from notification could choose to request spe- yield losses on their unfumigated 28.1 acres in Santa Cruz County to 60.4 cific notification of the exact date and strawberry acreage. acres in Ventura County. In Santa Cruz time at least 48 hours prior to the initia- Fields with more nonagricultural County, 54% of the fields were less than tion of fumigation. borders lost a larger percentage of their 25 acres, compared with only 24% in

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 43 ing Strawberry Advisory Board shows a decline in the 2001 freezer volume to 338.9 million pounds (or 25.7% of an- nual state production). This is below the previous 5-year average of 421.7 million pounds (30.5% of production). We estimate that about three-fourths of the total decline of 82.8 million pounds was due to the DPR regulations. This volume decline of almost 63 million pounds represents an estimated loss of Fig. 1. Hypothetical acreage loss for a 10-acre field due to 50-foot buffer. approximately 1 week’s production, on average, for every acre in the state. The revenue loss associated with this vol- Ventura County. Ignoring any system- data collected from actual permit ap- ume loss was approximately $10.4 mil- atic variations in field shape and the plications to determine the acreage lion for California growers. This is likely number of buffered sides, the differenc- for individual fields that could not be to be a conservative estimate, as some es in field size suggest that the impact fumigated due to inner buffer-zone re- growers lost much more than 1 week. of the buffer-zone regulations varied quirements. Using per-acre net revenue Additional fumigation days. The across counties. estimates from 2001 cost and return 2001 DPR regulations lengthened the For a given field size and buffer-zone studies by Klonsky and De Moura time period necessary for methyl bro- restriction, field shape also affected the (2001), we found that there was an in- mide fumigation for all growers in the share of nonfumigated acreage (fig. 1). dustry loss of $3.2 million due to the state. As indicated, the extent to which The three fields in the figure are each inability to fumigate acreage compris- the fumigation period was extended 10 acres. Each field has one side where ing inner buffer zones. varied by factors such as field shape, the adjacent property is in a nonagri- Processing-strawberry sales. On location, pounds of methyl bromide ap- cultural use, so that the inner buffer average, during the 4 years immediately plied and fumigation method. zone reduces the fumigated acreage. prior to the enactment of the 2001 DPR Total fumigation costs per acre in- For the square field (shape B), the inner regulations, approximately 417 million creased due to the diseconomies of fu- buffer-zone requirement reduces the pounds of California strawberries were migating relatively small pieces of land fumigated acreage by 7.6%. In contrast, sold annually to processors, about 30% each day, with additional costs such as for the rectangular field with a long of annual production. The 2001 DPR labor and equipment rentals. The dis- side bordering the nonagricultural use regulations significantly lengthened economies were more costly per acre (shape A), the inner buffer-zone require- the fumigation period, disrupting the for smaller fields. For instance, in Santa ment reduces the fumigated acreage by normal pattern of sales to the processing Barbara County it took one grower 9 10.7%. On the other hand, a rectangular market. The longer fumigation period days to fumigate a 9-acre field in 2001. field with a short side bordering a non- reduced sales to the freezer market, be- In the same county, it took another agricultural use (shape C) loses only cause growers had to remove the plants grower the same number of days to fu- 5.4% of its fumigated acreage. (In figure from the previous season earlier than in migate a 40-acre field. Based on grower 1, the long side is twice as long as the prior years, which reduced production. information and budget data, we esti- short side.) Some growers in Southern California mate that nonchemical fumigation costs Our analysis helped to clarify what lost up to 4 weeks of processing-market increased by at least 40% due to the lon- share in the effects of the regulations sales. Assuming 2,500 pounds per acre ger fumigation period. This translates across counties was due to differences per week of processing berries at the into a cost increase of about $400 per in field shape, and what share was 2001 average price of 30.6¢ per pound acre, resulting in an estimated industry due to differences in the proximity to (CPSAB 2001), the estimated revenue loss of about $10 million. In all likeli- residential areas and sensitive sites. We loss was $765 per acre per week. After hood, this is a conservative estimate of observed that growers in areas with harvest costs of about 14¢ per pound, the higher costs. higher population densities were much the gross profit on these sales would be Bed vs. flat fumigation. Due to more likely to be heavily affected by approximately $415 per acre per week regulatory specifications for emissions the buffer zone, permission and noti- or 16.6¢ per pound. ratios, the buffer-zone requirements fication requirements. Growers with Many growers reported that they were much more onerous for “bed” smaller fields faced a proportionately lost production at the end of the season fumigation, where only the raised beds greater loss of fumigated acreage than due to the 2001 DPR fumigation regula- are fumigated, than for “flat” fumiga- growers with large fields. We used tions. Data from the California Process- tion, where the entire field is fumigated

44 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 TABLE 2. Estimated statewide costs of 2001 DPR methyl bromide use restrictions to California strawberry growers

Cost $ (millions) Applying buffer zones 3.2 Lost processing-strawberry sales 10.4 Additional fumigation time 10.0 Switch from bed to flat fumigation 2.4 Notification 0.125 Total 26.125

(sometimes including multiple trips to find the neighbor at home). We valued the management/supervisor labor used for conducting notifications at $20 per hour, or roughly twice the cost of field labor. Together, these values indicate that the average per-acre notification costs were approximately $10, excluding mileage, copying and other costs. The overall notification cost was estimated by weighting the individual county es- After the methyl bromide rules were implemented, growers reported increased costs and lost income due to lower yields on untreated acreage, reduced sales to the freezer market, timates by production. This generated and additional labor, equipment and notification costs. an average cost of about $5 per acre, or $125,000 for the state. prior to bed construction. The scientific costs for county producers by about Where do the regulations stand now? studies consulted by the DPR indicated $700,000. The switching costs in Ven- that bed fumigation had a much larger tura County were estimated at about Impacts on growers are just one emissions ratio than flat fumigation, so $500,000 (500 acres); Monterey County, part of the regulatory environment for that human exposure to methyl bromide $700,000 (700 acres); Santa Cruz County, agricultural chemicals. A complex set of was much greater given the amount $300,000 (300 acres); and Orange Coun- political and legal processes came into of methyl bromide applied. In order ty, $200,000 (200 acres). Total switching play with the 2001 methyl bromide use to provide the same protection for hu- costs are therefore estimated to be ap- regulations, and cost-benefit analyses man health, larger buffer zones were proximately $2.4 million for 2001. that can be done using economic im- required for bed fumigation. Due to the Notification costs. Overall, our anal- pacts are just one part of the picture. In larger buffer zones and the associated ysis of the work-plan data indicated February 2002, San Francisco Superior loss of fumigated acreage, some grow- that notifications, and notification costs Court Judge A. James Robertson set ers found it preferable to switch to flat per acre, varied substantially across aside the regulations. He ruled that the fumigation. Flat fumigation is much fields. Smaller fields tended to have DPR improperly set up the regulations more expensive, however, at least an higher notification costs per acre. Fields and should have consulted with the estimated $1,000 per acre more than bed near urban areas or rural residential de- California Department of Food and Ag- fumigation. This regulation benefited velopments had a larger number of no- riculture before implementing them. pesticide applicators, because most tifications and higher notification costs The court ruling also imposed a new growers did not have the equipment per acre, on average. The estimated requirement that state agencies must necessary for flat fumigation and had to notification costs ranged from $1.67 per consider the economic impact of the hire custom applicators. acre in Santa Barbara County to $9.66 proposed regulations, although it is not Growers in Santa Barbara County per acre in Orange County. However, entirely clear that such consideration were most affected by the 2001 DPR reg- the Orange County estimates were will have any effect on regulations. In ulation. There are more than 3,000 acres based on a relatively small sample, so response, in 2002 the DPR introduced of strawberries grown in Santa Barbara those estimates may not accurately re- emergency regulations for methyl bro- County, and this acreage was virtually flect average costs per acre for all fields, mide application. A slightly revised all bed-fumigated prior to the growing and the Santa Barbara estimates ex- version of the 2001 regulations was season. In order to maintain economic cluded prefumigation 48-hour notices, permanently introduced in November viability, county producers switched underestimating per-acre costs. 2004 (see page 5). For the purposes of between 20% and 25% of these acres Based on information from grow- our analysis, the only notable difference from bed to flat fumigation in 2001, ers, the average notification required between the 2004 permanent regulations requiring a move to commercial ap- 30 minutes to prepare the paperwork and the 2001 temporary regulations is plicators and increasing application plus travel time to notify the neighbor that the minimum, inner buffer-zone

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 45 new pesticide regulations may contrib- ute to the increasing cost and difficulty of farming at the urban-rural interface, especially when agricultural areas are fragmented. If so, this type of regulation will encourage growers to stop farming at the interface, which may increase the rate of agricultural land conversion for residential and commercial construc- tion. Accordingly, such regulations may influence the spatial distribution of Cali- fornia agriculture and may reduce the Near Salinas, strawberry fields are directly adjacent to residential areas. If growers choose amount of open space remaining near not to farm at the rural-urban interface due to regulatory concerns, such agricultural lands California’s urban areas. could be at greater risk of conversion to residential or commercial uses. was reduced from 50 to 30 feet for very with small fields, were affected the most low emissions per acre and relatively on a per-acre basis. Differences in the C.A. Carter is Professor, J.A. Chalfant is small application blocks. estimated emissions of different ap- Professor and Chair, R.E. Goodhue is Asso- plication methods led to large per-acre ciate Professor, and G.J. McKee is Graduate Costs of regulation considered differences in the cost of the regulations Student, Department of Agricultural and State-level pesticide use regulations for different growers. Some growers Resource Economics, UC Davis. Carter, are intended to protect human health were forced to change their fumigation Chalfant and Goodhue are members of and the environment. Our analysis does method and hire commercial applica- the Giannini Foundation of Agricultural not imply that such regulations are not tors. In addition, grower costs increased Economics. The California Department of socially desirable, or that they are exces- because, in many cases, it took three to Food and Agriculture (CDFA) funded this sively costly when compared to their four times longer to fumigate each field. research. The opinions in this article are the benefits. Rather, it estimates the costs The extended fumigation period also authors’, not those of the CDFA. of a specific set of regulations and illus- reduced revenue from the processing trates how the cost burden of such regu- market for the old crop. References lations was distributed across growers. Apart from the direct evaluation of [CDFA] California Department of Food In many cases, such information can the industry costs of the 2001 methyl and Agriculture. 2002. California Department be used to suggest alternative sets of bromide use regulations, our analysis il- of Food and Agriculture Resource Directory. regulations that achieve the same health lustrates three general issues associated Sacramento, CA. 180 p. [CPSAB] California Processing Strawberry outcomes at a lower cost to growers. with use regulations. First, regulations Advisory Board. 2001. 2001 Annual Report. We conclude that the short-term that alter the timing of pesticide appli- Watsonville, CA. 18 p. impact of the 2001 DPR use regulations cation, by limiting acres or hours of ap- [DPR] California Department of Pesticide for methyl bromide to growers in the plicator exposure per unit of time, may Regulation. California Pesticide Information Portal. 2003. http://calpip.cdpr.ca.gov/cfdocs/ strawberry industry was significant, have costly indirect effects. In the case calpip/prod/main.cfm with the total estimated costs exceeding of strawberries, the harvest season was DPR. 2004. Status Report for Fumigant $26 million (table 2). The two most sig- truncated by the lengthened application Pesticides. Sacramento, CA. 6 p. www.cdpr. ca.gov/docs/dprdocs/methbrom/stat0704.pdf nificant components were the reduction period, which reduced industry rev- Federighi V. 2001. Regulating Pesti- in the volumes marketed for process- enues. Second, regulations that vary by cides: The California Story. California ing, due to the increased time needed application methods may have different Department of Pesticide Regulation, Cali- to fumigate for the following season, effects on the costs of different applica- fornia Environmental Protection Agency. Sacramento, CA. and increased fumigation costs. To the tion methods. In the case of strawber- Goodhue RE, Fennimore SA, Ajwa extent that growers found it difficult to ries, the buffer-zone specifications HA. In press. The economic importance implement a plan consistent with the resulted in so much lost acreage under of methyl bromide: Does the California DPR regulations, or difficult to arrange bed fumigation that many growers were strawberry industry qualify for a critical use exemption from the methyl bromide a fumigation schedule, we have under- forced to move to more-expensive flat ban? Rev Agric Econ. stated impacts on those growers. To the fumigation and hire commercial ap- Klonsky K, De Moura RL. 2001. Fresh extent that industry revenues increased plicators. Third, buffer-zone regulations Market Strawberries, Central Coast (Rep #ST-CC-01); Fresh Market, Freezer Strawber- due to reduced production, especially designed to limit human, nonapplica- ries, South Coast, Santa Maria Valley (Rep for processed strawberries, our estimate tor exposure will have unequal effects #ST-SC-01-1); Fresh Market, Freezer Straw- of increased costs overstates the effect of across growers. berries, South Coast, Ventura County (Rep the regulations on industry profits. The types of costs borne by growers #ST-SC-01-2). UC Cooperative Extension, and Department of Agricultural and Resource We found that the costs were un- provide an indication of those that may Economics, UC Davis. www.agecon.ucdavis. equally distributed across growers. accompany new restrictions on other edu/outreach/crop/archived-crop/strawber- Growers in urbanized areas, especially chemicals. Our findings illustrate that ries.htm

46 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 2004 Index

The following research articles, news stories Food insecurity prominent Plant sciences Courses help ranchers, farmers and editorials appeared in California Agriculture, among low-income California Aerial application of clopyralid mitigate water-quality impacts Volume 58, Numbers 1 through 4, January through Latinos — Kaiser et al. Jan-Mar demonstrates little drift poten- July-Sept p134 December 2004; numbers are Jan-Mar (1), Apr-June p18 tial and low toxicity to toads — DiTomaso et al. July-Sept Dairy workers learn husbandry, How can Californians be over- (2), July-Sept (3) and Oct-Dec (4). Back issues may p154 management skills July-Sept be purchased for $5 per copy, while supplies last; weight and hungry? — p135 Crawford et al. Jan-Mar p12 make checks payable to UC Regents. The complete HORTICULTURAL Nutritionists educate Vietnam- contents of all 2004 issues, including PDF versions Human and community BIOTECHNOLOGY ese immigrants about breast- feeding Oct-Dec p184 of research articles, can be found online at http:// development SPECIAL ISSUE: CaliforniaAgriculture.ucop.edu. Animal Ambassadors . . . Despite benefits, commer- Preventing Johne’s disease is 4-H teens learn to lead science cialization of transgenic good all-around dairy practice program for kids — Smith et al. horticultural crops lags July-Sept p137 Oct-Dec p209 — Clark, Klee, Dandekar Apr-June p89 Toll-free number aids Spanish- Horticultural biotechnol- Research and Project engages culturally di- * Biotechnology expands pest- speaking firestorm victims; UC ogy faces significant eco- review articles verse parents in Proposition 10 management options for reserve burns; staffer assists nomic and market barriers decisions — Campbell, Wright horticulture — Gianessi Apr- Latino victims Jan-Mar p6 Animal, avian, fisheries — Alston Apr-June p80 Jan-Mar p28 June p94 and veterinary * Diversity of horticultural * Transgenic trap crops and UC Berkeley’s Beahrs program biotech crops contributes Rural Latino families in Califor- an oasis for war-weary global Conserving California fish . . . rootstocks show potential to market hurdles — Brad- nia are missing earned income environmentalists Oct-Dec p185 Extension approaches applied — Driver, Castillón, Dan- ford, Alston Apr-June p84 tax benefits — Varcoe, Lees, to contentious marine-fisheries dekar Apr-June p96 * Transgenic produce slow to López Jan-Mar p24 management issues — Dewees, * Virus-resistant transgenic Perspective enter evolving global mar- Sortais, Leet Oct-Dec p194 papaya helps save Hawai- World trade rules affect horti- ketplace — Cook Apr-June Land, air and water ian industry — Gonsalves cultural biotechnology — Sum- In vitro gas production pro- p82 sciences Apr-June p92 ner Apr-June p77 vides effective method for Public-private partnerships Accuracy of cotton-planting assessing ruminant feeds — needed in horticultural forecasts assessed in the San Research updates Getachew, DePeters, Robinson research and development Joaquin Valley — Munier, Conventionally bred papaya still Jan-Mar p54 — Rausser, Ameden Apr- Goodell, Strand July-Sept p164 News possible, even in California Apr- June p116 June p74 Racing for crabs . . . Alternative techniques improve departments Costs and management op- Regulatory challenges irrigation and nutrient manage- EatFit guides adolescents to tions evaluated in Dungeness reduce opportunities for ment on dairies — Schwankl, Editorial overview improve health and fitness Jan- crab fishery — Dewees et al. horticultural biotechnology Frate July-Sept p159 Challenges and opportunities for Mar p10 Oct-Dec p186 — Redenbaugh, McHughen horticultural biotechnology — Autoguidance system operated * Race for Dungeness crab in- Apr-June p106 Bradford et al. Apr-June p68 “Pre-caucusing” improves labor fluences processing, markets at high speed causes almost no * China aggressively pursu- * Objectives for horticultural mediation Jan-Mar p8 — Hackett, Dewees, Krachey tomato damage — Abidine et biotechnology Apr-June p70 ing horticulture and plant al. Jan-Mar p44 Rural youth report more fre- Oct-Dec p190 * Glossary: Biotechnology Apr- biotechnology — Huang, quent smoking and drinking June p71 Tomato pomace may be a Rozelle Apr-June p112 Drip irrigation evaluated in Jan-Mar p9 good source of vitamin E in * IR-4 Project targets specialty Santa Maria Valley strawberries broiler diets — King, Zeidler crops — Holm, Kunkel Apr- — Hanson, Bendixen Jan-Mar Editorials Sustainable ag lectures online Jan-Mar p59 June p110 p48 ANR looks to the future — Jan-Mar p11 Gomes Oct-Dec p178 Weeds accurately mapped UC researchers evaluating Economics and using DGPS and ground- California’s growing diversity genetically engineered alfalfa public policy Food and nutrition based vision identification drives profound change — Apr-June p75 California handlers describe HORTICULTURAL — Downey, Giles, Slaughter Gomes Jan-Mar p2 * Pollen movement studied marketing issues for organic Oct-Dec p218 Apr-June p76 kiwifruit — Carman, Klonsky BIOTECHNOLOGY Water quality key to state’s SPECIAL ISSUE: July-Sept p169 Natural resources prosperity — Allen-Diaz, Frost Yo-yo dieting drives up obesity Consumer knowledge and July-Sept p130 Jan-Mar p11 Expanded production of labor- acceptance of agricultural Cattle grazing has varying impacts on stream-channel intensive crops increases agri- biotechnology vary — James Index 2003 Science briefs cultural employment — Khan, Apr-June p99 erosion in oak woodlands — George et al. July-Sept p138 Jan-Mar p63 Bush proposes immigration re- Martin, Hardiman Jan-Mar p35 * Consumers purchase Bt form Jan-Mar p4 sweet corn — James Irrigation and planting density Information for our HORTICULTURAL Apr-June p103 affect river red gum growth — Climate-change study predicts BIOTECHNOLOGY * Words matter — Cockerham Jan-Mar p40 contributors California water shortage Oct- SPECIAL ISSUE: Herrmann, Warland, Oct-Dec p222 Dec p183 Access to intellectual prop- Sterngold Apr-June p100 Long-term grazing study in Ecosystem approach for Klam- erty is a major obstacle to spring-fed wetlands reveals Introduction Davis school program supports ath fish Jan-Mar p4 management tradeoffs — Transgenic acreage grows amid developing transgenic horti- life-long healthy eating habits Allen-Diaz et al. July-Sept p144; changing regulation Apr-June cultural crops — Graff et al. in children — Graham et al. Feed supplement produces correction Oct-Dec p181 p72 Apr-June p120 Oct-Dec p200 heart-healthy milk Jan-Mar p5 * Nonprofit institutions Transparency tube provides * NRC recommends “biocon- form intellectual-property Diet, shopping and food-safety reliable water-quality mea- finement” measures Apr- No safe place to sit in tick- resource for agriculture skills of food stamp clients surements — Dahlgren, Van June p73 infested forests July-Sept p133 — Delmer Apr-June p127 improve with nutrition educa- Nieuwenhuyse, Litton July-Sept tion — Joy Oct-Dec p206 Radar maps soil moisture to cre- p149 Letters ate better wine Jan-Mar p5 Jan-Mar p4; Apr-June p79; July- Pest management Sept p132; Oct-Dec p180 Sudden oak death genome Low-toxicity baits control ants mapped July-Sept p133 in citrus orchards and grape Outreach news West Nile virus spreads July-Sept vineyards — Tollerup et al. Oct- California voters assess anti- p133 Dec p213 GMO initiatives Oct-Dec p182 * Sidebars.

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 47 COMINGUP

Special issue marks 40 years of Kearney research The Kearney Research and Extension Center is located southeast of Fresno in the central San Joaquin Valley, one

of the world’s most productive agricultural regions. This Courtesy of Manuel Jimenez unique center — UC’s most-utilized off-campus research facility — brings together diverse crops, complex facilities and world-renowned scientific expertise, including dozens of multidisciplinary researchers from throughout the UC Division of Agriculture and Natural Resources. Kearney’s mission is to provide state-of-the-science research and edu- cational programs to promote sustainability in California’s agricultural industry and enhance the quality of the ru- ral environment. The next issue of California Agriculture highlights important peer-reviewed research conducted at Kearney, ranging from new crop varieties and cultural and irrigation practices, to pest and disease management tech- niques, postharvest technology, air quality and molecular disease diagnoses.

At the UC Kearney Research and Extension Center, Visit California Agriculture on the Internet: research is developing sound information on culti- var selection and verifying production practices http://CaliforniaAgriculture.ucop.edu to assist Central Valley growers in establishing blueberries, a potentially lucrative specialty crop.

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48 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1