California Agriculture: Growing Bigger, Better

California Agriculture
JANUARYMARCH 2011
VOLUME 65 NUMBER 1
Growing bigger, better:

Artisan olive oil comes of age
University of California
Peer-reviewed Research and News in Agricultural, Natural and Human Resources
Editorial
Sustainable food systems: The global picture

The Merriam-Webster dictionary defines sustainable as of, relating to, or being a method of harvesting or using a resource so that the resource is not depleted or permanently damaged. For those of us engaged in agricultural research and extension, the term sustainability has often focused on farm-scale practices and solutions and regional food-system Dan Dooley issues. The rapidly emerging Vice President, Agriculture international view is that susand Natural Resources Senior Vice President, tainability must be considered External Relations in a global context, especially as it relates to food production, environmental and social protection, and climate change. Moreover, there is increasing awareness that intensive agriculture must and will play new roles in sustainable food systems, and that productivity gains from research, innovation, new technologies and education are essential. Feeding the world amid a changing climate forces us to critically review our traditional models and to realign our thinking with new priorities. We must recognize that enhancing food security and adapting to climate change go hand-in-hand. We must develop agricultural sustainability programs and policies that contribute to food security and climate change adaptation. We must develop technologies to sustainably produce more with less. Investment in research, development and delivery is a moral imperative. We already know that meeting local and global food demand will require diFeeding the world amid a changing climate forces us to verse production systems, and that those critically review our traditional models and to realign our systems must make key adaptations based on understanding the biology of climate thinking with new priorities. change, new pests and diseases, and crop mal products and meat. Higher temperatures, especially adaptations. We also know that the challenges for public in agriculturally important areas of the developing world, policy, resource management and science agencies are will reduce the yields of desirable crops, while changes in growing exponentially and intersect as never before. the amount and timing of precipitation will increase the For all segments of the University of Californias likelihood of short-term crop failures and long-term proDivision of Agriculture and Natural Resources, these duction declines. challenges offer both exciting opportunities to foster The message is clear. The historic challenges to proinnovation through research and outreach, and great duce safe and abundant food and fiber, to address poverty responsibility to align our priorities with those iswhile safeguarding the environment and guiding sussues where we have the greatest potential to make the tainable energy development, and meanwhile to stimulate biggest difference. economic growth and jobs, must all now be assessed in the context of climate change and the need for sustainable Find links to resources for this editorial at: development at the global level. http://ucanr.org/repository/CAO/issue.cfm?issue=current
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CALIFORNIA AGRICULTURE VOLUME 65, NUMBER 1
orldwide, public and private investments in agriculture and natural resources research benefitting our food systems have been enormously successful. These investments have fostered innovation and new technology, improved food security and human nutrition, developed new tools to maintain essential natural ecosystems, and generated economic benefits to producers, processors and consumers alike. Looking ahead, however, many signs point to the sobering reality that our current pace of innovation and gains in agricultural productivity will not be enough. By 2050, the world population will top 9 billion people. Most of that growth will come in the worlds developing countries. Improving dietary standards in rapidly developing economies like China and India have already increased demand for calories and protein, putting upward pressure on world cereal and oilseed prices while also increasing volatility in world markets. From a natural resources perspective, the United Nations estimates that in order to meet nutrition goals, world demand for water for irrigation will double by 2050, while demand for forest products is expected to increase 40% by 2060. Perhaps most compelling, global food demands are expected to double by the middle of the century. At the same time, our understanding of the expected impact of global climate change points to more stress on the global food system. Populations in the developing world, already vulnerable to food insecurity, will likely be the most seriously affected. The International Food Policy Research Institute (IFPRI) just published a study on the impact of climate change on global agriculture, which suggests that climate change will result in additional price increases for the worlds most important agricultural crops: rice, wheat, corn and soybeans. Increasing crop prices will in turn put upward pressure on feed, ani-
TABLE OF CONTENTS
JANUARYMARCH 2011 VOLUME 65 NUMBER 1
Growing bigger, better: Artisan olive oil comes of age

Research and review articles
8 UC Cooperative Extension sensory analysis panel
enhances the quality of California olive oil
Vossen and Kicenik Devarenne
COVER: The California olive industry has undergone striking changes in recent years. An internationally certified sensory taste panel has raised the quality of California olive oils, creating new markets (page 8); the nonnative, invasive olive fruit fly has transformed pest control for oil and table olives (pages 14, 21 and 29); and super-high-density hedgerow plantings have contributed to increased oil olive acreage (page 34). Photo: Lisa Romerein.
Sensory panel data continues to be essential to the evolution and growth of the California olive oil industry.
14 Understanding the seasonal and reproductive

biology of olive fruit fly is critical to its management
Burrack et al.
A statewide monitoring program has provided valuable insights on the olive pests occurrence, population dynamics, reproduction and other factors.
21 Biological controls investigated to aid management

of olive fruit fly in California
Daane et al.
News departments
5 Letters
H. White joins Cal Ag, CSIT staff
Researchers studied the biology of imported natural enemies to determine the best species to release in the states climatically varied olive-growing regions.
6 Research news
New methods are transforming table olive and olive oil production in California Campus trees yield olive oil, body-care products
29 High temperature affects
olive fruit fly populations in Californias Central Valley

Johnson et al.
Adult flies suffer from heat stress in very hot weather, and their ability to fly, feed and reproduce is affected.
29
47 2010 index
34 Mediterranean clonal selections evaluated for

Tous et al.
modern hedgerow olive oil production in Spain

Three olive oil cultivars were tested for their horticultural characteristics and sensory qualities in super-high-density fields.
For more information on California olives and olive oil health benefits, visit California Agriculture: http://californiaagriculture.ucanr.org
39
Olive cultivars field-tested in super-highdensity system in southern Italy

Godini, Vivaldi, Camposeo
Editors note:
Thank you to more than 10,000 subscribers who have renewed their subscriptions! At the end of January, we will purge our mailing list. You can still renew for a short time or start a new subscription at: http://californiaagriculture.ucanr. org/subscribe.cfm
41 Methods evaluated to minimize emissions from preplant soil fumigation

Gao et al.
Low permeability plastic mulches are highly effective but costly; water treatment or target-area fumigation are better options for crops with low profit margins.
The olive engravings used throughout this issue are from The Olive in California by Byron M. Lelong, published in 1888 and reprinted in Californias Olive Pioneers (Robert Mondavi Institute for Wine and Food Science, 2009).
http://californiaagriculture.ucanr.org JANUARYMARCH 2011 3
Über uns
California Agriculture is a quarterly, peer-reviewed journal reporting research, reviews and news, published by the Division of Agriculture and Natural Resources (ANR) of the University of California. The first issue appeared in December 1946, making it one of the oldest, continuously published, landgrant university research journals in the country. The print circulation is currently about 15,000 domestic and 1,800 international, with a strong online presence. Mission and audience. California Agricultures mission is to publish scientifically sound research in a form that is accessible to a well-educated audience. In the last readership survey, 33% worked in agriculture, 31% were faculty members at universities or research scientists, and 19% worked in government agencies or were elected office holders. Indexing. The journal is indexed by AGRICOLA; Current Contents (Thomson ISIs Agriculture, Biology and Environmental Sciences, and the SCIE databases); Commonwealth Agricultural Bureau (CAB) databases; EBSCO (Academic Search Complete); Gale, including Lexis-Nexis; Google Scholar; Proquest; and others, including open-access databases. It has high visibility on Google and Google Scholar searches. We post all peer-reviewed articles to the California Digital Librarys eScholarship Repository. Authors and reviewers. Authors are primarily but not exclusively from ANR; in 2008, 15% were based at other UC campuses, or other universities and research institutions, and 13% in 2009. In 2008 and 2009, 14% and 50% (respectively) of reviewers came from universities and research institutions or agencies outside ANR. Rejection rate. Our rejection rate ranged between 20% and 25% in the last three years, In addition, associate editors and staff sent back 24% of manuscripts for revision prior to peer review. Peer-review policies. All manuscripts submitted for publication in California Agriculture undergo double-blind, anonymous peer review. Each submission is forwarded to the appropriate associate editor for evaluation, who then nominates three qualified reviewers. If the first two reviews are affirmative, the article is accepted. If one is negative, the manuscript is sent to a third reviewer. The associate editor makes the final decision, in consultation with the managing and executive editors. Editing. After peer review and acceptance, all manuscripts are extensively edited by the California Agriculture staff to ensure readability for an educated lay audience and multidisciplinary academics. Submissions. California Agriculture manages the peer review of manuscripts online. Please read our Writing Guidelines before submitting an article; go to http:/ /californiaagriculture.ucanr.org/submit.cfm. Letters. The editorial staff welcomes your letters, comments and suggestions. Please write to us at the address below. Include your full name and address. Letters may be edited for space and clarity. Subscriptions. Subscriptions are free within the United States, and $24 per year abroad. Single copies are $5 each. Go to http:/ /californiaagriculture. ucanr.org/subscribe.cfm or write to us. International orders must include check or money order in U.S. funds, payable to the UC Regents. MasterCard/Visa accepted; include complete address, signature and expiration date. Permissions. Articles may be reprinted, provided that no advertisement for a commercial product is implied or imprinted. Please credit California Agriculture, University of California, citing volume and number, or complete date of issue, followed by inclusive page numbers. Indicate [[year]] The Regents of the University of California. Photographs in print or online may not be reprinted without permission.
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Letters
UC plant pathologist on cover
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WHAT DO YOU THINK? The editorial staff of California Agriculture welcomes your letters, comments and suggestions. Please write to us at: 1301 S. 46th St., Building 478 - MC 3580, Richmond, CA 94804 or [email protected]. Include your full name and address. Letters may be edited for space and clarity.
We lived on a 30-acre farm in the heart of Editors note: For the cover of the October-December Pescadero in San Mateo County, and artichokes 2010 issue (The Golden State goes gray: What aging were his main crop. My father was born in Jackson, will mean for California), we ran a stock image of seAmador County, on March 24, 1912. My grandnior runners at Lake Tahoe. The image was posted on parents moved the family back to Italy when dad Shutterstock with no information identifying the runwas about 14 months old, ners. We were delighted to receive the following letter. and then came back to America when he was 17 Thats my father on the cover! so that he wouldnt lose My father is Donald C. Hildebrand, who was a his citizenship. He arrived plant pathologist at UC Berkeley until about 1992. with 16 cents in his pocket. He earned his Ph.D. there but is now retired. He He made it to Half Moon and several collaborators Bay and worked on farms, named three new bactemarried my mother Mary rial species that affected Neves from Pescadero plants, and published a in 1941. They moved to paper showing for the first Santa Cruz, where he and time that crown gall of a friend trucked produce October 1973 California plants could be cured. up and down the coast for Agriculture article on Several years ago I ata few years and then went artichoke varieties tended a dinner with him into farming again. at UC Berkeley, where he He had a Brussels sprouts farm in Davenport was honored for donatfor 3 or 4 years and then purchased the 30 acres in ing enough money from Pescadero and planted artichokes. He harvested October-December 2010 the family to establish the them from fall to spring and then cut down the California Agriculture Hildebrand-Laumeister plants and waited for the crop to produce again in Chair in Plant Pathology. the fall, which was the norm for raising artichokes This picture was taken last year by my sister, at that time. After a few years, he began stumpKarin Hildebrand Lau of Sacramento, at a relay race ing the artichokes, removing the dried stalks that in Tahoe. He was 77 in that photo. He now resides had produced the buds and leaving room for new in Sisters, Ore., and will be 79 in a few months. He growth. He increased his annual production from still actively runs every chance he can and is quite about 275 boxes to 500 boxes per acre. He worked an inspiration! The runner with his back to the with Richard (Hank) Sciaroni, keeping charts on camera is Joe McCladdie, another member of the the barn door as to whatever he was doing, and did Lake Merritt Joggers & Striders Over 70 team. this with a 3-year school education (in Italy). Thank you so much for choosing such a wonder- Martha Giannini Muzzi Moss Landing ful cover. This is certainly the way I will always remember him.
Katie Hildebrand OConnor Granite Bay
Father doubles artichoke yields
Editors note: We received the following letter regarding Joseph Giannini, a grower from Pescadero who co-authored an article in the October 1973 issue, Magnifico...a promising new globe artichoke variety, with Vincent E. Rubatzky, Richard H. Sciaroni and Marvin J. Snyder. My father, Joseph Giannini, is now 98 years old, and we are putting together a booklet of all he quietly accomplished in the farming of Brussels sprouts and artichokes. Thank you for providing copies of the article that he published in California Agriculture.
California Agriculture is pleased to announce that Hazel M. White has been hired as part-time senior editor. White will split her time between California Agriculture journal and the publications unit of Communication Services and Information Technology (CSIT), with responsibility for proofreading, copyediting, indexing and writing. White has more than 20 years of experience in editorial work, with a focus on gardening and horticulture. She served as managing editor for a new edition of the Sunset Hazel M. White Western Garden Book, and continues to write Sunset magazines monthly What to do in your garden feature. She is the author of 11 books, and has written numerous newspaper and journal articles on gardening, landscaping, sustainability and urban farming. White can be reached at [email protected].
Nancy Warner
H. White joins Cal Ag, CSIT staff
Research news
New methods are transforming table olive and olive oil production in California
live production is evolving rapidly in California. The states traditional, laborintensive table olive culture is giving way to super-high-density, mechanically harvested plantings of the fruit for oil. The next decade could see California producing a significant amount of the olive oil consumed in the United States, says UC Cooperative Extension (UCCE) farm advisor Paul Vossen, whose work has helped cultivate California olive oil as a unique and growing agricultural market (see page 8). Meanwhile, scientists are closing in on a mechanical harvesting system for table olive trees that could save the industry from being crushed by oppressively expensive hand-labor harvesting costs.
A long and storied history
Olives are the most extensively cultivated crop in the world. Below, Lucca, a new variety developed at UC Davis, grows in a test plot.
Native to the Mediterranean region, olive cultivation began some 7,000 years ago for use as food, a beauty aid, in ceremonies and as fuel. The utility of olives is chronicled in ancient Egyptian hieroglyphics, Greek mythology, the Bible and Quran, Shakespeares sonnets and innumerable cookbooks, old and new. Today, olives are the most extensively cultivated fruit crop in the world. In 1769, the first olive cuttings were planted in California at the Mission San Diego. During the 1800s, many small olive plantations existed around the state, but a statewide industry didnt emerge until German immigrant Freda Ehmann of Oroville, working with Professor Eugene Hilgard of UC Berkeley, perfected the ripe-olive curing process at the turn of the century. Canned black olives (which producers market as black-ripe olives) became a quintessential California product. Mild, versatile and meaty, California olives flavor pizza and Mexican dishes and appear on relish trays and in tapenade. Currently, California has about 27,000 acres in table olive production, the bulk in Tulare, Tehama, Glenn and Butte counties. Canning olive tonnage has declined in the past 5 years, but the price per ton has been steadily improving. In 2006, farmers harvested 123,589 tons of canning olives valued at $700 per ton, but in fall
2009, 23,034 tons were harvested valued at $1,200 per ton. Just two major canneries process California table olives: Bell Carter Olive Company in Corning and Musco Family Olive Company in Tracy. The harvest runs from September to November, with crews climbing ladders to hand-pick the thousands of olives on a typical tree, labor that consumes 45% to 60% of table olive producers gross returns. UC Davis plant sciences specialist Louise Ferguson is working with a team of farm advisors to develop mechanical harvest methods for table olives, a particularly challenging task because of the high quality standard. There is zero tolerance for bruised fruit in the canned product, Ferguson says. The scientists are studying two options trunk shaking and canopy contact but both have problems. With age, the trunks of olive trees become stout, fluted and knobby, which hinders mechanical shaking. Canopy contact is complicated by harvest timing. The fruit must be harvested before it is fully ripe, so significant force is required to remove them from the tree. Both methods now produce acceptable olives with about 65% harvesting efficiency, Ferguson says. However, with some tree pruning and the development of a suitable conveying and catching platform for the harvesters, I believe that machines could be commercially available in 2 years.
Olive fruit fly
Alexandra Kicenik Devarenne
Olive fruit fly is a severe threat to all California olives. A pest for at least 2,000 years in Mediterranean olive production, it first appeared in California in 1998 and quickly spread to all commercial olive-growing regions in the state (see pages 14, 21 and 29). The female olive fruit fly lays her eggs in immature fruit. After they hatch, feeding larvae destroy the pulp and introduce microbes that rot the fruit. For table olives, the presence of even a few infested fruit can lead to rejection of the entire crop. Oil olives can tolerate some infestation, as long as the fruit are not rotten.
Super-high-density orchards
During the last century, most of the olive oil used in California was imported from Spain and
Karin Higgins
Italy. Interest in local products, greater awareness about the health benefits of olive oil, and a growing appreciation for fine olive oils unique flavor has buoyed the California olive oil industry. In traditional olive orchards, about 50 trees per acre were often planted 30 feet apart, giving them plenty of space to reach their full natural size. Productive orchards have been maintained in some parts of the world for 100 years or more. But scientists, interested in boosting yield per acre, reducing labor costs and bringing olive plantations into full production quickly, have developed a new, superhigh-density, hedge-row olive production scheme (see page 34). About 10 years ago, Spanish investors planted Californias first super-high-density olive plantation near Oroville. The idea took off. Theyve introduced super-high-density all over the world Chile, Australia, Portugal, says Joe Connell, UCCE farm advisor for Butte County. The method was developed by a nursery near Barcelona, the largest olive nursery in the world. You can imagine the potential sales for a nursery when producers need more than 600 trees per acre to establish an orchard. In addition, older olive tree trunks and branches become woody and gnarled, characteristics that will interfere with mechanical harvesting. The super-high-density orchards being established now may have to be removed and replaced in just 15 to 20 years, Connell says. According to a 2009 UC Davis Olive Center survey, 12,137 acres of super-high-density olive trees were planted in California by the end of 2008, with 92% of growers reporting that they planted the trees between 2005 and 2008. Many of the plantations are coming into production right now. Dan Flynn, director of the Olive Center, says California olive oil production numbers are experiencing parallel growth. In 2008, California produced 650,000 gallons of olive oil, and in 2009, 800,000 gallons. In 2010, olive oil production will exceed 1 million gallons. Theres a lot of high quality California oil this year, Flynn says. California olive oil will be more readily available around the country.
Developing markets for olive oil
Californias young olive oil industry uses up-todate farming and pressing methods to make oils altogether different from European oils, whose producers are following the practices and traditions of the Old World. Fine California olive oils taste asspicy, peppery and pungent as the olives from which they were made. California olive oils are not just fats, but are like spices or condiments, says Sonoma County olive oil expert Vossen. These fine olive oils impart delicious, subtle flavors to food. With dozens of olive varieties at their disposal, a diversity of climate and soil types, and unconstrained by tradition, California producers are only now beginning to explore the range of flavors that can be coaxed from fine olive oil. Flavors range from the green end of the spectrum, with green apple, grass and green tea, to the ripe end, with buttery, nutty and tropical flavors. And they can be found everywhere in between, Flynn says. Or, you can find all these flavors wrapped up in one very complex olive oil. Jeannette Warnert
UC President Mark Yudof (right) examines the UC Davis Olive Centers Presidents Blend olive oil, with UC Davis Chancellor Linda Katehi.
Campus trees yield olive oil, body-care products

UC Davis has been producing olive oil from its more than 2,000 olive trees since 2005, keeping the olives which used to clutter the ground out of the waste stream while generating revenue for teaching and research at the UC Davis Olive Center. The center recently launched its Presidents Blend olive oil, and teamed up with UC Davis alumna Kacie Klein to produce a collection of olive-oil-based bodycare products including lotion, body butter, hand-cut soap and lip balm. These new products are all made with olive oil produced by the campuss historic olive trees, using olives and olive oil that would otherwise have gone to waste, says Dan Flynn, executive director of Olives from the UC Davis the Olive Center. The product sales support research into new olive cul- campus, which once littered the ground, are now used to tivars, mechanical harvesting, olive produce body-care products. fruit fly control, olive processing and the sensory evaluation of olive oil. Olives have the potential to be one of the leading crops in the state, with UC Davis being a leader in the industry, just like with wine and almonds, UC President Mark Yudof said. UC Davis olive products are sold in the UC Davis Bookstore and can be ordered online from the its Campus Produced section at: http:/ /ucdavisbookstore.com/MerchList/ aspx?ID=16472&CatID=3016. Editors
Nicole Sturzenberger
Developing a market for the oil will be important to the industrys success. Currently, more than 99% of the olive oil consumed by Americans is imported from other countries. Imported oil is generally cheaper and blander than the oil pressed by Californias artisan producers, Flynn says. In addition, an Olive Center study found that 69% of the imported oils sampled from California groceries had sensory defects. This study rocked the olive oil world, Flynn says.
REVIEW ARTICLE
UC Cooperative Extension sensory analysis panel enhances the quality of California olive oil
by Paul M. Vossen and Alexandra Kicenik Devarenne
Californias olive oil industry has evolved from primarily a salvage operation of the table olive industry to a producer of worldclass, pre mium, extravirgin olive oil. In 1997, UC Cooperative Extension started the first California olive oil taste panel, which was officially recognized by the International Olive Council in 2001. Specific protocols were used to screen potential panelists and train them to identify defects and positive characteristics, identical to 43 other
California sensory panel members evaluate oils at an official tasting.
Interest in planting new orchards is still high, but the economic crisis has world taste panels. The UCCE panel reduced the rate of oil-olive acreage helped the California Olive Oil Council growth. A few large producers make about 80% of the states olive oil, but develop a seal certification program more than 90% of the farms are small using sensory analysis. Certification scale with less than 20 acres. Production provides consumers with assurance of premium olive oil in California is predicted to double in the next 3 years that labeled oils are free of defects and warrant the extra virgin grade. from 800,000 to 1.6 million gallons. Many of these oils are excellent, taking Sensory evaluation using a unique top awards in global competitions. UCCE profile sheet provides complete But this was not always the case. The improvement in Californias olive oil and detailed information about spe is due largely to the efforts of a sciencific positive flavor characteristics of tifically selected and trained sensory olive cultivars grown in California. evaluation panel. Only the most ruThe UCCE sensory panel has also dimentary quality testing on olive oil is currently being done by laboratory contributed to a better understand ing of the qualities of California olive chemical analysis; a group of human beings following strict tasting protocols oil and advancement of the industry is now the standard tool for detecting, by participating in research on pest identifying and quantifying the many positive and negative attributes of management, cultural practices and olive oil. processing. Although people have been making and using olive oil for thousands of years, the methodical sensory uring the California olive oil reanalysis of olive oil is a recent develvival of the past two decades, a opment. Its use in measuring qualquiescent industry has come dramatiity was advanced significantly in the cally to life (see box, page 9). Acreage early 1980s, when sensory researchers planted in oil olives is increasing rapin Spain, Italy, Greece, Portugal and idly. By fall 2010, an estimated 28,500 France began working together with acres were growing in California, a the International Olive Oil Council doubling of acreage from 3 years prior. (now the International Olive Council or
IOC) to develop the first official tasting methodology. Their work applied the principles of sensory science to olive oil. Sensory evaluation evokes, measures, analyzes and interprets the responses of tasters to the flavors they perceive. Worldwide, sensory analysis has become a key part of how olive oils are rated for market grade, and it has been used to help growers and processors produce a higher-quality product. Since the late 1980s, many researchers have used sensory evaluation to characterize olive oil flavors attributable to cultivar (variety), fruit maturity, terroir, irrigation, tree nutrition, pest damage, fruit handling and processing methods. Researchers have also taught sensory short courses and workshops for industry professionals and consumers about olive oil styles and quality.
Uses of a sensory panel
A trained sensory panel is an invaluable tool. It provides an objective sensory evaluation of olive oil that can be used by regulators to enforce label standards that protect consumers, producers and processors from fraud in the industry. IOC quality standards are used globally to determine whether an oil should be graded and marketed as extra virgin or virgin, or refined and then sold as olive oil (see box, page 10). In order for an oil to be graded as extra virgin, it must pass several
laboratory chemical analyses and be evaluated by a sensory panel. The olive oil must be free of defects and have some fruitiness. Official IOC tastings that rate oils for compliance to trade standards note the intensity of any defects. Only three positive attributes fruitiness (either green or ripe fruit), bitterness and pungency are quantified on the profile sheet. The official IOC profile sheet includes five standard defects: fusty/ muddy sediment, musty, wineyvinegary, rancid and metallic. Space is left to note negative attributes other than the classic defects (IOC 2006, 2007c). Beyond evaluating by defined IOC standards, sensory panels help producers make better decisions regarding variety selection, pest management, cultural practices and harvest timing. With qualitative analysis, processors can also better select processing methods to maximize quality and assess how various cultivars might contribute desirable characteristics in blends.
Sensory evaluation in research
Variety. Sensory panels define the attributes of olive varieties and rate them according to the intensity of fruitiness, bitterness and pungency, but also provide an in-depth evaluation of fruit flavor characteristics. The content of volatile aromatics (aroma compounds emanating from the oil) and polyphenols (complex phytochemicals that act as antioxidants) make up much of an oils flavor, and are highly variable between varieties. Qualitative analysis of the fruity characteristics of an olive oil provides valuable information about the sensory contributions of different cultivars, helping producers to select varieties and market product to consumers (Cimato et al. 1996; Romero et al. 2005; Tura et al. 2000; Uceda and Aguilera 2005; Vossen 2003, 2007a, 2007d). Fruit maturity. Fruit ripeness can have a significant influence on the oils flavor. Immature fruit produces oils with green fruity flavors such as freshcut grass, herbs, artichoke or mint. More mature fruit yields oils with ripe notes such as nutty, buttery, floral, apple, banana, berry or tropical. Sensory analysis of oils made from greener fruit has shown high bitterness and pungency, which correlates with laboratory
analysis showing high polyphenol and antioxidant levels (Alba Mendoza et al. 1997; Romero and Daz 2002; Vossen 2005). Terroir. Climate, soil composition and other environmental factors that make up terroir may influence olive oil qualities, but this is a continuing area of research. Most scientists have indicated that the influence of terroir is minimal compared to variety and
fruit maturity, but some studies have shown that oils from different areas are notably different in flavor (table 1). Sensory characteristics have also been used to identify oils by protected growing region (appellation) (Aparicio et al. 1997; Ranalli et al. 1999; Tous et al. 1997; Vossen 2007c). Irrigation. Irrigation is the most commonly manipulated grower practice that specifically influences oil sensory
The sensory aptitude of potential tasters is screened by having them arrange oils along a scale for particular attribute intensities.
Olive oil in California

The olive came to California from Mexico with the Franciscan fathers. Although olive oil production likely started within a couple of decades of the 1769 founding of the first California mission in San Diego, the earliest written record is from 1803. After a period of decline in the mid-1800s, olive oil production expanded between 1870 and 1900; the states first commercial olive oil mill is believed to have been established in Ventura County in 1871. Unable to compete with low-priced oil from Europe, around 1900 the California olive industry turned its attention to table olive production. Table olives dominated the domestic olive scene for more than 75 years. For years, the California olive oil industry was largely a salvage operation, using culls from table fruit production to produce low-quality oil for refining. In the late 1980s, a small number of growers began to produce high-quality olive oil for the gourmet market. Some of these early producers harvested existing trees that had been regarded mostly as messy ornamentals for years. But other growers, for the first time in decades, planted olives with the intention of producing oil. Acreage of table olives declined during the same period, primarily because of competition from inexpensive imports in the Californiastyle black olive market. A 2004 survey of the California olive oil industry found 528 growers in 38 counties, producing almost 400,000 gallons of oil on 6,170 acres. From 2005 to 2008, another 13,400 acres were planted, and in the last 2 years an estimated 9,000 more have gone in, mostly in super-high-density orchard systems (see page 34). California olive oil currently represents only 2% of domestic consumption, so there is a vast market to be tapped. Since the domestic industry is producing extra-virgin olive oil that is as good as imports, consumer education and the enforcement of quality standards may be key elements in capturing more of the domestic market. For more information go to: http://cesonoma.ucdavis.edu.
qualities (table 2). Large flavor differences have been documented in oils from trees given different amounts of irrigation water (ranging from 15% to 107% of seasonal need). Droughtstressed trees tend to produce excessively bitter and pungent oils. Trees maintained with a moderate water status (controlled deficit) tend to produce oils with higher overall fruitiness that is balanced with bitterness and pungency. Heavily watered trees generally produce bland olive oils with little fruitiness or pungency (Berenguer et al. 2006; Salas et al. 1997). Olive fruit fly. Sensory evaluation of oils made in California from fruit with different levels of olive fruit fly damage showed that the conventional 10% threshold was often too conservative, and too generic to predict senory impacts. In blind sensory evaluations, no significant flavor differences could be detected in fresh oil from early damage by fly larva prior to the onset of
soft fruit rot, even when fruit was 100% damaged. In 2008, however, the sensory panel found that off flavors could immediately be detected when fruit rot ranged from 1% to 5%. Therefore, with early harvest and rapid processing, minor olive fruit fly damage can be tolerated, which can save treatment costs and reduce environmental contamination (Hermoso et al. 2001; Vossen, unpublished data; Vossen and Kicenik Devarenne 2006a). Harvest, transport and storage. Most olive oil defects come from improper handling of the fruit during and after harvest. If the fruit is compromised in any way, it should be milled within 24 hours of harvest. This includes broken skins, storage at temperatures above 40F (5C) or fermentation beginning in piled fruit (Garca et al. 1996). Washing and leaf removal. In Italy and Spain, researchers found that when fruit was clean and dry (unwashed), it produced oils with a consistently better
sensory rating than if clean and wet (washed) due to the lower moisture content of the paste. Normally, all leaves are removed, but researchers found that some leaves (up to 3%) left in the olives during crushing gave the oil more bitterness, green fruitiness and green color. This could be desirable if these characteristics are lacking (Hermoso Fernndez et al. 1991; Di Giovacchino et al. 1996). Crushing. Differences in paste characteristics have been demonstrated to produce various effects on oil sensory quality. Finer pastes tend to release more oil that possesses greener color and stronger herbaceous, grassy, sweet almond and cypress wood flavors. Coarse paste tends to produce less bitter and pungent oils (Di Giovacchino 1996; Koutsaftakis et al. 2000). Malaxation. Changing the time, temperature and amount of oxygen exposure during malaxation (slow mixing) of olive paste influences the oils
TABLE 1. Sensory attributes of Arbequina olive oils grown in three different zones in Spain Attribute Fruity Green Bitter Pungent Sweet Sensory rating* Siurana 2.4 1.5 1.1 1.6 1.8 7.7 Garrigues 2.2 1.4 1.8 1.7 1.8 7.4 Andaluca 3.1 1.8 0.6 0.6 2.4 8.9
Olive oil definitions and regulations

Extra virgin and virgin. Extra virgin is a grade of olive oil narrowly defined by the International Olive Council (IOC). Its standards require oil to be produced entirely by mechanical means, without the use of solvents, under temperatures that will not degrade the oil (less than 86oF [30oC]). It must have a maximum free-fatty-acid level of less than 0.8% (an indication of the fruits condition) and a peroxide value of less than 20 milliequivalent O2 (a measure of oxidation). Most importantly, a trained and IOC-recognized sensory evaluation panel must find it free from defects and possessing some degree of fruitiness. The next grade of olive oil is virgin, which may have a free-fatty-acid level up to 2% and some slight flavor defects. Common and lampante. The grades common and lampante (lamp oil) are lower still, for oil possessing more pronounced defects. Lampante oil must be refined before it is usable. While these standards are widely recognized in the United States, there is no guarantee that an oil labeled extra virgin meets IOC standards. In October 2010, new voluntary USDA standards for olive and olive pomace oil went into effect, essentially adopting the IOC laboratory and sensory standards. California, Connecticut and Oregon have done the same at the state level. Hopefully, these new standards will be broadly adhered to The California Olive Oil Council awards the extra-virgin certification seal to member oils in the United States to protect both that are defect free. consumers and ethical producers.
* European Union rating scale, 09 points. Source: Tous et al. 1997.
TABLE 2. Means of sensory characteristics of oils from trees receiving different amounts of irrigation Treatment (% ETc)* 15 25 40 57 71 89 107
Fruity 3.60a 3.20a 2.70b 2.60b 2.10c 1.80c 1.70c
Bitter 6.00a 4.20b 1.70c 0.93d 0.30d 0.22d 0.20d
Pungent 4.90a 3.90b 1.90c 1.10d 0.30e 0.22e 0.20e
* Evapotranspiration rate (water use by olive trees) with a coefficient corrected for olive trees compared to a general reference rate. Different letters indicate values significantly different at P = 0.01. Source: Berenguer et al. 2006.
10
sensory characteristics. Longer malaxation times increase oil yield, lower polyphenol levels and lower the levels of aromatic volatiles responsible for some fruity flavor characteristics. Raising the paste temperature causes greater extraction of polyphenols, but every 22F (12C) increase in temperature doubles the loss of volatile aromatics. Paste malaxed at 95F (35C) produces oil that is sharply bitter compared with at 77F (25C). Malaxation tanks that exclude oxygen significantly increase bitterness and pungency. Many researchers are currently investigating the effects of low oxygen exposure on aromatic compounds that influence fruitiness (Angerosa 2002; Di Giovacchino et al. 2002; Hermoso Fernndez et al. 1991). Extraction system. Press systems have consistently produced oils with more defects than continuous-flow systems. Sensory evaluation of oil from continuous-flow processing systems that use different amounts of added water have shown that oils are higher in fruitiness, bitterness, pungency and green character when less water is added (Alba Mendoza et al. 1996; Hermoso Fernndez et al. 1998; Kicenik Devarenne and Vossen 2007a).
Oil styles and excellence recognition.
Providing industry professionals with accurate evaluations of olive oil flavor characteristics is extremely important. With flavor profiles of their oils, producers can make well-informed decisions about the styles of olive oils they want to produce, and consequently, better olive oils. UC Cooperative Extension (UCCE) has produced several informative handouts on how to define extravirgin olive oil and interpret an olive oil label, and how untrained tasters can inadvertently promote the use of defective oils. Many untrained tasters are average consumers who are accustomed to defective flavors, identifying them with the taste of olive oil (Kicenik Devarenne and Vossen 2007b; Vossen 2007a; Vossen and Kicenik Devarenne 2006b).
The California sensory panel
During a 1996 study leave, farm advisor Paul Vossen realized that Europeans understood olive oil quality and were using sensory analysis to describe and promote positive characteristics. They were also using sensory analysis to
weed out poor-quality oils and educate producers about defects, to help them avoid making production mistakes. In 1997, the first California screening for sensory panel members was conducted at UC Davis, with the aid of Juan Ramon Izquierdo from the Spanish Arbitration Laboratory Olive fruit fly is a major pest of olives. The sensory effects of in Madrid. Using IOC infestation depend on both the quantity and type of damage. procedures, potential panelists were screened for olfactory UC Davis Olive Oil Taste Panel, recently and gustatory sensitivity and also for certified by the IOC.) motivation, availability and personalTasting protocols ity (IOC 2007a). Twenty people out of 75 Samples are presented blind and were selected. Subsequent screenings added another 26 panelists. Altogether, in the most appropriate order, so that errors of contrast are minimized (see 46 tasters were selected out of 217 applicants (21%). About half of those have box, page 12). Oils are identified with a random three-digit number or letter chosen to remain active. combination that is not familiar in any Trained panel members minds and way, to prevent order bias. Special blue palates must become calibrated over glasses are used to obscure the oil color, time to an absolute scale of intensities so that color bias does not influence the for all the common flavor attributes of panelists evaluations, and tasters are olive oil. The calibration process takes isolated from one another with dividseveral years and is not permanent; panelists must continually receive train- ers. For the most accurate evaluation, oling if they are to remain sharp. Training ive oils are warmed to 80F (26.5C) on a is conducted by a panel leader who pro- warming mat. Because flavors based in vides the group of tasters with samples oil coat the mouth, throat and nasal cavof known characteristics and intensities ity, they tend to linger, which influences the reaction to subsequent samples and in order for them to learn and rememquickly fatigues the senses. A resting ber specific positive and negative attime of 5 minutes is required between tributes. Panelists must also taste oils oils, and green apples and water are from all over the world to learn the used as palate cleansers to minimize characteristics of each variety, so that sensory fatigue. Panelists usually taste varietal differences are not confused from three to five oils in 30 minutes with defects. (IOC 2007c). The IOC recognizes sensory panels Sensory panelists place a short, vertithat are approved by a government cal mark on a horizontal, unstructured, agency such as the U.S. Department of 10-centimeter line scale where the flavor Agriculture. Panels from around the intensity is perceived to be. Data on world take compulsory proficiency profile sheets containing individual oil tests called ring tests, in which they all ratings is compiled by a technician and taste and rate the same five oils. The analyzed with a statistical computer results are compared using a standard program developed by the IOC. The procedure that is analyzed statistically software places each oil into a specific for variability, accuracy and uniforcategory extra virgin, virgin, commity. In 2001, the UCCE sensory panel participated in a series of ring tests and mon or lampante based on the IOC standards for defect-intensity levels and became one of 41 officially recognized the presence of fruity characteristics. IOC taste panels, the first one in the The minimum IOC sensory definiUnited States to have received such tion of an extra-virgin oil, for example, recognition (IOC 2007b). (Many of the original tasters are now members of the is one in which the mean score of the
eight panelists is zero defects with some fruitiness. This means that five out of eight must agree in their profile-sheet characterizations. If the coefficient of variation (relative robust standard deviation) of the main defect is greater than 20% in a defective oil, or greater than 10% in an extra-virgin oil for the fruitiness characteristic, the test must be repeated. Tasters must be very close in identifying the primary defect in each oil, if it has one, and the intensities of the defect must be within 2 points on the 10-centimeter scale. For fruitiness, the intensity must be within 1 point on the scale. The statistical program makes a calculation (median, interquartile interval, robust standard deviation, relative robust and standard deviation) based on each panelists evaluation of each oil, and a minimum of eight panelists must be used for an official oil evaluation (IOC 1999).
UC and the olive oil industry
The International Olive Council conducts ring tests, sending the same five oils to panels around the world for testing to ensure that its standards are being upheld.
In 1999, the California sensory panel began providing feedback to the states olive oil industry in the form of a seal certification program, in partnership with the California Olive Oil Council
(COOC), a trade organization. UCCE farm advisor Vossen was responsible for training the sensory panel and maintaining scientific protocol. The COOC seal was awarded to oils that the sensory panel judged extra virgin according to IOC standards. Producers also benefited from panelist comments regarding their oils characteristics. If an oil failed certification, the farm advisor confidentially informed the producer of the nature of the defect and its
How to taste olive oil

Olive oil is best tasted in a blue, tulip-shaped, stemless glass. The tasting glass is covered with either a lid or hand, and the oil gently swirled. The open glass is placed close to the nose and the taster takes a deep breath, making a mental note of the aroma, since much of what we call flavor is actually smell. Next, the taster sips about 5 milliliters of oil and holds it in their mouth for 10 seconds, Blue glasses are used to taste olive oil, in order to taking care to coat all parts of prevent color bias. the mouth and tongue. While the oil is in the mouth, air is sucked in to further volatilize its aromatic components before swallowing. Then the mouth is closed while the taster breathes out through the nose. The retronasal cavity connecting the mouth to the olfactory area allows the volatile aromas to be perceived once again. The mouth and throat detect flavors such as bitterness, pungency, sweetness and astringency. Most people taste bitterness primarily toward the back of the tongue and mouth. Pungency is a physical irritation perceived in the throat, which is why it is essential to swallow some of the oil in order to appreciate all of its sensory characteristics.
likely cause. From 1999 through 2004, the number of defective oils dramatically declined from 50% to less than 3%. If an oil was deemed defect-free (and therefore certifiable) but there was room for improvement, the panels comments regarding harvest maturity or other factors were passed along to the producer. The COOC seal was the first attempt by the domestic industry to give consumers an assurance of quality when purchasing California olive oil. In 2005, a new UCCE profile sheet was developed for more detailed analysis of extra-virgin olive oils in California. It records taster impressions of additional aspects, including the oils harmony and complexity. By selecting from a list of descriptors such as artichoke, banana, almond or fresh-cut grass, the tasters note undertones in the olive oil. Previous sensory panel analysis emphasized defect identification. Descriptive analysis provides extremely valuable data on the more subtle and complex aspects of olive oil. This can help producers adjust harvest timing, tailor processing methods to particular varieties and pinpoint attributes for blending. UC has also been addressing the needs of the California olive oil industry with training programs, such as the 2-day Olive Oil Sensory Evaluation Short Course, taught once or twice per year since 1999. Likewise, special trainings have been conducted for chefs, food writers, producers, consumers and educators. In addition, UCCE short courses on olive production
12
topics, regional grower meetings and field days have also provided valuable science-based information. Two UC Division of Agriculture and Natural Resources publications, the Olive Production Manual and Organic Olive Production Manual, continue this tradition.
This will help growers select varieties that are horticulturally suited to their location. Ongoing research on how olive fruit fly can damage the sensory aspects of olive oil will help producers further adjust their pest control measures to minimize environmental and financial impacts, while preserving oil quality. A research project comparing Looking to the future different processing systems will proDue to UC research and support, and vide valuable information for producers the efforts of the sensory panel volunseeking the best methods for their parteers, it has become a rarity to find deticular fruit, depending on variety and fects in a California olive oil. Research ripeness. continues to explore the effect of terroir The UCCE sensory panel is providon olive oil, and a database is being cre- ing feedback on specific flavor charated of characteristics in single varietal acteristics of individual oils that helps oils grown in different parts of the state. producers to choose varieties, adjust
References
Alba Mendoza J, Hidalgo F, Casado MA, et al. 1996. Caractersticas de los aceites de olive de primera y segunda cetrifugacin. Grasas Aceites 47(3):16381. Alba Mendoza J, Izquierdo JR, Gutirrez Rosales F. 1997. Aceite de Olive Virgen Anlisis Sensorial. Editorial Agrcola Espaola, S.A. Artes Grficas COIMOFF, S.A. Madrid, Spain. Angerosa F. 2002. Influence of volatile compounds on virgin olive oil quality evaluated by analytical approaches and sensory panels. Eur J Lipid Sci Technol 104:63960. Aparicio R, Morales MT, Alonso V. 1997. Authentication of European extra-virgin olive oils by their chemical compounds, sensory descriptors and consumer attitudes. J Agr Food Chem 45:104683. Berenguer MJ, Vossen PM, Grattan SR, et al. 2006. Tree irrigation levels for optimum chemical and sensory properties of olive oil. HortScience 41(2):42732. Cimato A, Baldini A, Caselli S, et al. 1996. Observations on Tuscan olive germplasm. 3: Analytical and sensory characteristics of single-variety olive oils. Olivae 62:4651. International Olive Oil Council, Madrid, Spain. Di Giovacchino L. 1996. Influence of extraction systems on olive oil quality. Olivae 63:5263. International Olive Oil Council, Madrid, Spain. Di Giovacchino L, Angarosa F, Giacinto D. 1996. Effect of mixing leaves with olives on organoleptic quality of oil obtained by centrifugation. J Am Oil Chem Soc 73:3714. Di Giovacchino L, Costantini N, Ferrante ML, et al. 2002. Influence of malaxation time of olive paste on oil extraction yields, chemical and organoleptic characteristics of virgin olive oil obtained by a centrifugal decanter. Grasas Aceites 53:17986. Garca JM, Gutierrez F, Castellano JM, et al. 1996. Influence of storage temperature on fruit ripening and olive quality. J Agr Food Chem 44:2647. Hermoso Fernndez M, Gonzles J, Uceda M, et al. 1998. Elaboracin de aceite de oliva de calidad II Obtencin por el sistema de dos fases. Manual from the Estacin de Olivicultura y Elaiotecnia. Finca Venta del Llano Mengbar (Jan), Spain. Junta de Andaluca Vol 61. Hermoso Fernndez M, Uceda M, Garca-Ortiz A, et al. 1991. Elaboracin de aceite de oliva de calidad. Manual from the Estacin de Olivicultura y Elaiotecnia. Finca Venta del Llano Mengbar (Jan), Spain. Junta de Andaluca Vol 5. Hermoso JF, Romero A, Tous J, et al. 2001. Incidencia del sistema de recoleccin en la calidad del aceite de oliva en el sur de Catalua. IV Congreso Ibrico de Ciencias Hortcolas. Cceres, Mayo. p 201220. [IOC] International Olive Council. 1999. Organoleptic assessment of virgin olive oil computer program Excel file statistical analysis. COI/T.20/Doc No 15/Rev. 1. IOC. 2006. Trade standard applying to olive oils and olive pomace oils. COI/T.15/NC No 3/Rev 2, Nov 24, 2006. IOC. 2007a. Guide for selection, training and monitoring of skilled olive oil tasters. COI/T.20/Doc No 14/Rev 2, Sept 2007. IOC. 2007b. Guidelines for the accreditation of sensory testing laboratories with particular reference to virgin olive oil according to standards ISO/IEC 17025:2005. COI/T.28 Doc No 1, Sept 2007. IOC. 2007c. Sensory analysis of olive oil method for the organoleptic assessment of virgin olive oil. COI/T. 20/Doc No 15/ Rev 2, Sept 2007. Kicenik Devarenne A, Vossen PM. 2007a. A report on California experiments with different olive oil mills. Proceedings-abstracts of Beyond Extra Virgin: Italo-Californian Olive Oil Conference, UC Davis, May 22-23. California Institute of Food and Agricultural Research. p 34. Kicenik Devarenne A, Vossen PM. 2007b. Cooks Illustrated, Dec. 2006: Comparison of olive oils revisited. Handout Proc Sensory Evaluation of Olive Oil short course, September 28-29. UC Davis Extension. Koutsaftakis A, Kotsifaki F, Papamanolioudaki A, Stefanoudaki E. 2000. Effect of olive crushing parameters on the qualitative characteristics of virgin olive oil. In: Vitagliano C, Martelli GP (eds.). Proc 4th Intl Symp Olive Growing. Acta Hort 586. Ranalli A, De Mattia G, Batumi M, Proietti P. 1999. Quality of virgin olive oil as influenced by origin area. Grasas Aceites 50(4):24959. Romero A, Daz I. 2002. Optimal harvesting period for Arbequina olive cultivar in Catalonia (Spain). In: Vitagliano C, Martelli GP (eds.). Proc 4th Intl Symp on Olive Growing. Acta Hort 586. Romero A, Tous J, Guerrero L. 2005. Caracterizacin sensorial del aceite Capitulo 15. (Banco de Germoplasma de Catalua.) In: Rallo L, et al. (eds.). Variedades de Olivo en Espaa (Libro II: Variabilidad y seleccin). Junta de Andaluca, MAPA y Ediciones Mundi-Prensa, Madrid.
harvest maturities, schedule irrigation and generally improve the quality of their oils. California-specific data produced by the sensory panel using internationally recognized scientific standards and methods will continue to be essential to the growth of the California olive oil industry.
Paul M. Vossen is Farm Advisor, UC Cooperative Extension, Sonoma and Marin counties; and A. Kicenik Devarenne is Freelance Olive Oil Consultant, Writer and Educator, Sonoma County. Shermain D. Hardesty, Specialist in the UC Davis Department of Agricultural and Resource Economics, served as Guest Associate Editor for this article.
Salas J, Pastor M, Castro J, Vega V. 1997. Influencia del riego sobre la composicin y caractersticas organolpticas del aceite de oliva. Grasas Aceites 48(2):7482. Tous JM, Romero A, Plana J, et al. 1997. Chemical and sensory characteristics of Arbequina olive oil obtained in different growing areas of Spain. Grasas Aceites 48(6):41524. Tura D, Failla O, Bassi D, Serraiocco A. 2000. Sensory and chemical analyses of monovarietal olive oils from Lake Garda (Northern Italy). In: Vitagliano C, Martelli GP (eds.). Proc 4th Intl Symp on Olive Growing, Valenzano, Italy. Acta Hort 586:5958. Uceda M, Aguilera M. 2005. Caracterizacin sensorial del aceite. Capitulo 15. (Banco de Germoplasma Mundial de Crdoba.) In: Rallo L, et al. (eds.). Variedades de Olivo en Espaa (Libro II: Variabilidad y seleccin). Junta Andaluca, MAPA y Ediciones Mundi-Prensa, Madrid. Vossen PM. 2003. California Arbequina and Arbosana olive oils get a very high rating from the local tasting panel. OLINT Mag 2:15 (special English ed.). Vossen PM. 2005. Variety and maturity: The two largest influences on olive oil quality. UNICO website Italian American Service Organization. http:// cesonoma.ucdavis.edu/files/27177.pdf. Vossen PM. 2007a. Core issues grant report: Californias unique olive oil identity. https://ucanr.org/cig/ programs/programswork/annualreportview.cfm. Vossen PM. 2007b. Olive oil: History, production and characteristics of the worlds classic oils workshop. Mediterranean fruits: Ancient history andmodern promise. HortScience 42(5):1093100. Vossen PM. 2007c. Orchard practices and olive oil quality. Proceedings-abstracts of Beyond Extra Virgin: Italo-Californian Olive Oil Conference. UC Davis. May 22-23. California Institute of Food and Agricultural Research. p 23. Vossen PM. 2007d. Site, varieties and production systems for organic olives. In: Organic Olive Production Manual. UC ANR Pub 3505. Oakland CA. Vossen PM, Kicenik Devarenne A. 2006a. Comparison of mass trapping, barrier film and spinosad bait for the control of olive fruit fly in small-scale orchards and landscapes in coastal California. Proc Olivebioteq 2:26774. Marsala, Italy. Vossen PM, Kicenik Devarenne A. 2006b. What is extra virgin olive oil? The vocabulary of an olive oil label. Handout Proc Sensory Evaluation of Olive Oil short course, September 28-29, UC Davis Extension.
REVIEW ARTICLE
Understanding the seasonal and reproductive biology of olive fruit fly is critical to its management
Jack Kelly Clark, UC Statewide IPM Program
by Hannah J. Burrack, Ray Bingham, Richard Price, Joseph H. Connell, Phil A. Phillips, Lynn Wunderlich, Paul M. Vossen, Neil V. OConnell, Louise Ferguson and Frank G. Zalom
The olive fruit fly was first detected in Los Angeles in 1998 and in all the olivegrowing regions of California soon after. Following its initial detec tion, UC researchers and Cooperative Extension farm advisors, county agricultural commissioners and the California Department of Food and Agriculture Pest Detection and Emer gency Project established a statewide monitoring program to determine the extent of the olive fruit flys occur rence, track its seasonal biology and evaluate monitoring tools. Fly popu lations and infestations can reach high levels throughout California but tend to be lower in the San Joaquin Valley. Trap captures typically exhibit a bimodal distribution with peaks in the spring and fall. Olive infestation is related to fly densities, climate and fruit size. Gravid, mated females vary in density throughout the year but are present at some level yearround. The data is being used to develop models that will better predict when the adults are active and olives are at risk.
First detected in 1998, the olive fruit fly spread quickly throughout the states olive-growing regions. The table olive industry has zero tolerance for damaged fruit, but infestation levels of 10% or more may be acceptable for olive oil. Above, the adult flys exit holes; larvae feed just below.
he olive fruit fly was first detected in California in 1998 in the Los Angeles Basin and was subsequently found in all olive-growing areas within 4 years (fig. 1). The olive fruit fly (Bactrocera oleae [Rossi]) is the primary pest of olives worldwide and is particularly troublesome due to its multiple, overlapping generations each year. This life history makes understanding olive fruit fly phenology and infestation patterns
14
particularly important for effective management. The insects historic range includes all of Europe and Africa, and extends at least as far east as India (Augustinos et al. 2002; Nardi et al. 2005). Molecular studies of B. oleae in California suggest that the invasion originated from Mediterranean populations. Australia is the only country where olives are grown that is not colonized. In the traditional olive-growing regions of Europe and the Middle East, the olive fruit fly is the primary economic pest. B. oleae has become the most important pest of California olives (Collier and Van Steenwyk 2003; Daane et al. 2005), and in commercial production control necessitates regular applications of insecticidal bait sprays from fruit-set through harvest. The majority of Californias crop is processed for table olives and is grown in the Sacramento and San Joaquin valleys, in Butte, Glenn, Tehama and Tulare counties (Connell 2005). Olive oil is also produced from California olives. At the onset of the olive fruit fly invasion, oil production occurred primarily in coastal counties, including Napa and Sonoma. In recent years, oil production has been increasing in the traditional
table oliveproducing counties. B. oleae is managed differently in these two production systems: there is zero tolerance for infestation in table olives, while a threshold of roughly 10% infestation is acceptable for oil olives, although even greater levels can produce high-quality oil if the fruit is processed quickly (Kicenik Devarenne and Vossen 2007). This production difference is particularly notable in Butte County, where high fly densities and associated damage resulted in crop rejection by table olive processors. Consequently, olives grown in Butte County are crushed for oil. Super-high-density oil plantings have been established in Butte County since 1999. These plantings in which olive trees are spaced more closely, varieties with smaller fruit are planted and deficit irrigation is used appear to be less conducive to olive fruit fly infestation (Vossen 2007) (see page 34).
Statewide monitoring program
We and other researchers were interested in understanding the seasonal activity patterns of B. oleae in California as compared to its previously known range, in order to predict where and when the fly was most likely to become a significant pest. In 2002, UC
researchers and Cooperative Extension farm advisors, California Department of Food and Agriculture Pest Detection and Emergency Project personnel, county agricultural commissioners and pest control advisers assembled a network of monitoring sites throughout the state, in order to determine olive fruit fly population dynamics within and between Californias diverse climatic and geographic regions. A network of 28 monitoring sites in 16 counties was established and data was collected from 2002 through 2006 (table 1). This large dataset allowed us to track B. oleae activity patterns and to relate these patterns to fly and fruit biology. The end-product of this work will be predictive models for fly activity and fruit infestation. Because the initial goal of this monitoring effort was to track B. oleae seasonal biology, sites with active, relatively large populations were selected, and all traps were placed in olive plantings that received no insecticide applications for the duration of the study. Therefore, all population fluctuations observed were due to local biotic and abiotic factors, not anthropogenic effects. The selection of untreated sites with large B. oleae populations led to a lack of locations in the San Joaquin Valley, because most olive plantings in this area are used for commercial table olive production and may be treated with pesticides if B. oleae are present. In addition, other researchers documented that populations in the San Joaquin Valley appear naturally lower than coastal and Sacramento Valley locations (Rice et al. 2003; Yokoyama et al. 2006). The olive fruit fly had already been detected in 35 counties prior to 2002. After the monitoring program was initiated, it was found in nine more counties (fig. 1), although the detection years do not necessarily indicate initial invasion. This is particularly clear in the case of Colusa County, which was surrounded by counties in which the fly had been detected, but for which there were no records of olive fruit fly until 2004.
Geography and seasonal activity
Del a spiroketal pheroNorte Siskiyou Modoc mone lure attractive to males (Yokoyama et al. 2006). Plastic Trinity Shasta Lassen Humboldt McPhail traps Tehama (Liquibaitor trap, Plumas Mendocino Glenn Butte Great Lakes IPM, Sierra a ba ad Colusa Vestaburg, Mich.) Yu Nev Placer Lake baited with an aqueEl Dorado Yolo Sonoma Sacra Napa Alpine ous torula yeast food mento a d o r s Am ra Solano ve ala lure attractive to both C Tuolumne Contra San Costa Joaquin San Francisco sexes were shown to s Alameda lau Mariposa nis San Mateo ta be more attractive than Santa S Clara Merced Santa Cruz ChamP traps (Burrack et Madera San al. 2008), and in 2003 all Fresno Benito monitoring locations beMonterey Kings gan to use two to four of the McPhail traps. San Luis Obispo Every week the traps were checked, flies were counted and Santa Barbara sexed, and lures were changed. Trapping was conducted from April through December at most locations, with a subset of locations (Butte 1, Napa 1, Napa 2, Napa 3, Napa 4, San Diego 1, San Luis Obispo 2, Solano 4, and Yolo 1) continuing year-round. Weekly trap
Sut ter
1998 1999 2000 2001 2002 2004
Fig. 1. Years of initial olive fruit fly detection in California counties.
TABLE 1. Olive fruit fly monitoring locations, geographic classifications and years active County Amador Butte Calaveras Marin Napa Site 1 1 1 1 1 2 3 4 Sacramento 1 2 3 4 San Diego San Luis Obispo Santa Barbara Shasta Solano 1 1 2 1 2 1 1 2 3 4 Sonoma Tulare Ventura Yolo Yuba 1 2 1 1 1 1 No. of traps 4 4 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 4 2 2 4 4 4 2 Geographic area North, inland North, inland North, inland North, coastal North, coastal North, coastal North, coastal North, coastal North, inland North, inland North, inland North, inland South, coastal South, coastal South, coastal South, coastal South, coastal North, inland North, inland North, inland North, inland North, inland North, coastal North, coastal South, inland South, coastal North, inland North, inland 2005 2002, 2003, 2004, 2005 2002, 2003, 2004, 2005 2002, 2003, 2004 2002, 2003, 2004, 2005, 2006 2002, 2003, 2004, 2006 2002, 2003, 2004, 2006 2002, 2003, 2004, 2006 2002, 2003, 2004 2005 2004 2004 2002, 2003, 2004, 2005 2002, 2003, 2004, 2005, 2006 2002, 2003, 2004, 2005, 2006 2004 2004 2002, 2003, 2004, 2005 2002, 2003, 2004 2002, 2003, 2004, 2005, 2006 2002, 2003, 2004 2002, 2003, 2004, 2005, 2006 2002, 2003, 2004, 2005 2003, 2004, 2005, 2006 2005 2005 2002, 2003, 2004, 2005, 2006 2003, 2004 Years active
Ma
rin
Mono
Inyo Tulare
Kern San Bernardino Ventura Los Angeles
Orange
Riverside
San Diego
Imperial
Statewide monitoring began using four ChamP yellow sticky traps per site baited with ammonium bicarbonate food lures attractive to both sexes and
captures were converted to flies per trap per day to allow for comparison between locations. Flies per trap per day were summed, divided by the number of locations reporting data for the week, and graphed to allow observation and comparison of population density trends. Olive fruit fly flight activity has a bimodal distribution, with the highest trap captures observed in spring and fall (fig. 2A). Depending on location, spring peaks occur in March, April or May and fall peaks are in September, October or November. The majority of Yellow sticky traps, left, are used to monitor the flys population densities in different locations throughout the year. Right, an adult olive fruit fly caught in a trap. the pooled trapping data points represented at least 15 monitoring sites (fig. 2B), except for the winter dates. Overall 40 A fly activity was low in the winter, 35 and the locations selected for winter 30 monitoring were among those with the 25 highest B. oleae trap captures during the 20 15 previous summer and fall. Flies were 10 still present during winter at these loca5 tions, but were trapped in lower num0 bers. Trap captures were lower in 2002 than in subsequent years, likely due to 25 the use of a less efficient trap and the B 20 shorter time since initial B. oleae establishment in more northern locations. 15 When sites were grouped into broad 10 geographic categories, differences in seasonal activity became apparent. We 5 considered a trapping site to be coastal 0 if it was either in a county directly borJuly Oct Jan Apr July Oct Jan Apr July Oct Jan Apr July Oct Jan Apr July Oct Jan dering the ocean or west of the summit 2002 2003 2004 2005 2006 of the coastal mountain range. Coastal locations have milder climates than Fig. 2. (A) Average flies per trap per day caught at all monitoring locations over 4 years and (B) number of trapping locations reporting each week. those inland, with cooler summers and warmer winters. We considered trapping locations to be northern when 100 they were situated at greater than 37 90 N latitude (roughly Santa Cruz), with Inland 80 the remainder categorized as southern. Coastal Both coastal and inland locations in70 cluded sites with very high (10,000 or 60 more flies; San Diego, Butte and Solano 2) and very low (under 1,000 flies; Marin 50 and Tulare) trap captures (table 2). Trap 40 data from the same geographic areas 30 was pooled and graphed. The sites from Northern and 20 Southern California displayed similar 10 activity patterns and are not presented, 0 but fly trap capture patterns at inland July Oct Jan Apr July Oct Jan Apr July Oct Jan Apr July Oct Jan Apr July Oct Jan versus coastal locations differed mark2002 2003 2004 2005 2006 edly (fig. 3). The pooled inland locations exhibited similar bimodal trap Fig. 3. Flies per trap per day caught at combined inland and coastal trapping locations over 4 years. capture patterns to those observed for
16
Flies/trap/day by site Sites reporting Flies/trap/day by site
Alexandra Kicenik Devarenne
Jack Kelly Clark
combined data from all sites (fig. 2A), but pooled coastal locations lacked a spring peak and displayed a gradual increase of fly captures, with the greatest numbers captured in the fall (fig. 3).
Tracking olive infestations
Olive infestation and olive size were tracked in 2004 and 2005 at seven locations, and fly density was tracked during 2005. Manzanillo and Mission olives, the most commonly grown varieties in California (Connell 2005), were sampled at most locations, and Leccino olives were sampled at one location because no suitable Manzanillo or Mission olives were available (table 3). One hundred olives were collected weekly from four trees at each location, June through December 2004, and May through December 2005. Sample size was decreased to 52 olives per tree when fruit infestation reached 50%. Olives were dissected under a stereomicroscope, and oviposition scars (stings), live larvae, and pupae or larval/adult exit holes were counted. Olives bearing stings were considered infested, as table olive producers have a zero tolerance policy for olive fruit fly infestation. Prior to dissection, each olive was measured to compare fruit size across locations, because olive fruit fly adults exhibit a preference for large fruit under field conditions (Burrack and Zalom 2008; Yokoyama et al. 2006). The longest point on the olive (l), the widest point (w) and 90 from the widest dimension (h) were measured and used to calculate fruit volume (V = (4/3)(h/2)(w/2)(l/2)). Fly populations were monitored at each location using four plastic McPhail traps, as described previously. Data from 2004 and 2005 was similar for all locations, therefore data from 2005 is presented. Infestation levels in 2005 reached 100% in Butte and Ventura counties. Infestations grew slowly at the Amador and Sonoma sites but were high by the end of the season (fig. 4A). Fly trap captures mirrored the delayed infestation pattern at Amador and Sonoma (fig. 4B), and these two locations had the smallest olives throughout the season (fig. 4C). Smaller olives are typically less infested in the field (Burrack and Zalom 2008), and both fly population and olive size are affected by weather. Infestation
levels and trap captures were low in Tulare County for the entire season, despite olive size and development comparable to the other monitoring locations (figs. 4A, 4B and 4C). Previous monitoring efforts have also reported lower trap captures in
San Joaquin Valley locations (Rice et al. 2003; Yokoyama et al. 2006). B. oleae populations in the Central Valley may be limited by high temperature and food resources (Wang et al. 2009) (see page 29). Solano County Mission olives were significantly less infested than
TABLE 2. Total olive fruit flies caught at monitoring locations during olive production season (May through November) in 2003, 2004 and 2005* County Amador Butte Calaveras Marin Napa Site 1 1 1 1 1 2 3 4 Sacramento 1 2 3 San Diego San Luis Obispo 1 1 2 Santa Barbara 1 2 Shasta Sonoma 1 1 2 Solano 1 2 3 4 Tulare Ventura Yolo Yuba 1 1 1 1 No. of traps 4 4 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 4 4 4 4 2 2003 3,880 406 331 3,499 1,459 1,920 1,001 8,711 3,765 52 1,857 602 8,216 10,466 4,051 1,167 2,454 1,163 2004 10,956 4,692 78 2,039 2,459 3,034 3,397 6,988 6,838 5,290 1,227 3,756 3,924 3,979 204 4,895 1,207 11,667 40,422 9,490 9,914 7,521 2005 10,718 8,487 1,369 2,942 10,008 1,191 2,339 1,700 3,058 1,288 16,686 2,889 287 13,800 5,269
. . . . . . . . . . . . . . . . . number of flies . . . . . . . . . . . . . . . . .
* Data from 2002 and 2006 not presented because data collection was not season-long. Winter dates and years with incomplete data for a location are omitted.
TABLE 3. Olive infestation data locations County Amador Butte Sonoma Solano Tulare Ventura Yolo Location Abandoned orchard Commercial and fallow orchard Abandoned orchard Wolfskill Experimental Orchard Lincove Research Station Abandoned orchard UC Davis campus farm Trapping location Amador 1 Butte 1 Sonoma 2 Solano 4 Tulare 1 Ventura 1 Yolo 1 Varieties sampled Leccino Manzanillo, Mission Mission Manzanillo, Mission Manzanillo Mission Manzanillo, Mission
Manzanillo olives from the same location. Field observations from this site suggest that Manzanillo olives may be preferable to Mission for oviposition in the field when female flies have a choice (Burrack and Zalom 2008).
Reproductive biology
Examination of trap captures compared to ovarian development in the female indicated that the olive fruit fly has at least four generations per year in California, with a partial generation spanning the winter (Burrack 2007). An absence of mature eggs in fly ovaries during the spring and early summer has often been noted in European B. oleae populations (Delrio and Prota 1976; Economopoulos et al. 1982; Fletcher et al. 1978; Raspi et al. 2002; Tzanakakis 1986) and is referred to as a summer reproductive diapause. A similar absence of mature eggs can be induced in flies reared in the laboratory by exposing larvae to cool, short days and adults to hot, long days with no
(A) Fruit infested
100 90 80 County, variety Amador, Leccino Butte, Manzanillo Solano, Manzanillo Solano, Mission Sonoma, Mission Tulare, Manzanillo Ventura, Mission Yolo, Manzanillo
access to olives (Koveos and Tzanakakis 1990, 1993; Koveos et al. 1997; Raspi et al. 2002; Raspi et al. 2005). In order to determine if this phenomenon occurs in California B. oleae populations as well as to determine when flies were capable of infesting olives, females flies collected from monitoring traps were dissected for five sites (Butte 1, Napa 1, San Diego 1, Solano 4 and Yolo 1). These locations were selected because trapping was conducted yearround, and they represented different California climates. Ten flies from each location and sampling date were dissected, and when fewer than 10 flies per week were collected, all flies were dissected. Ovarian development, egg load and mating status were observed for each of the dissected flies. We determined whether the ovaries of female flies contained mature eggs and whether their spermathecae contained sperm. Mature eggs are easily distinguished from developing eggs by a distinctly darker micropile on the anterior end. Egg load, or the total number of mature eggs present in both
Fruit infested (%)
70 60 50 40 30 20 10 0
5/12
6/12
7/13
8/13
9/13
10/14
11/14
Fig. 4. (A) Percentage of fruit infested, sampled weekly, (B) flies caught per trap per day and (C) olive development at fruit infestation locations in 2005. Gaps in lines signify dates for which olive data was not collected. (C) Olive volume
5,000 4,500 4,000
ovaries, was also determined. Mating status was determined via staining with 4, 6-diamidino-2-phenylidole dihydrocholride (DAPI) at 1 microgram per milliliter in phosphate buffered solution and observed with UV-flourescent microscopy as adapted from Fritz and Turner (2002). Flies were dissected in 70% ethyl alcohol, and spermathecae were removed, placed in a drop of DAPI on a microscope slide and crushed with a cover slip. The morphology of the olive fruit fly spermatheca and ethanol preservation made quantification of sperm difficult. Therefore, flies were classified as mated or unmated. An overall classification of reproductive biology was assigned to each fly by combining ovarian development rankings and mating status. These categories were: (1) unmated (sperm absent), immature (immature ovaries); (2) unmated, mature (mature ovaries); (3) mated (sperm present; mature eggs in ovaries [gravid]), immature; and (4) mated, mature. Only flies in category 4 would be capable of infesting olives. All statistical analyses were conducted using SAS version 9.1 (SAS Institute, Cary, N.C.). Analysis of variance was conducted with Proc GLM, and means were separated via LSD. Nonparametric rank tests were conducted using the Kruskal-Wallis test via Proc Npar1way in SAS. There were significant differences between months in the proportion of unmated flies with immature ovaries and mated flies with mature ovaries observed (unmated/immature: F8,20 = 5.16, P = 0.0014; mated/mature: F8,20 = 4.94, P = 0.0018), but there was also a significant site/month interaction for
(B) Flies per day

140 120 100 80 60 40 20 0 5/12 County Amador Butte Solano Sonoma Tulare Ventura Yolo
Olive volume (mm3)
Total ies/trap/day
3,500 3,000 2,500 2,000 1,500 1,000 500
County, variety Amador, Leccino Butte, Manzanillo Solano, Manzanillo Solano, Mission Sonoma, Mission Tulare, Manzanillo Ventura, Mission Yolo, Manzanillo
6/12
7/13
8/13
9/13
10/14
11/14
0 5/12
6/12
7/13
8/13
9/13
10/14
11/14
18
both categories (unmated/immature: F32,20 = 4.01, P = 0.0009; mated/mature: F32,20 = 5.17, P = 0.0001). The differences among years for both rankings were nonsignificant (unmated/immature: F2,20 = 2.36, P = 0.1205; mated/mature: F2,20 = 1.18, P = 0.3267), and therefore, yearly data was pooled by month. Because of the significant interaction effect between site and month, the data for individual sites is presented. The greatest proportion of mated, mature flies was observed in March or April and October through November, for the Yolo, Solano and Butte county sites (figs. 5A, 5B and 5C). High proportions of potentially destructive flies (mated, mature) were observed in April, August and September in Napa County (fig. 5D). The greatest proportion of unmated, reproductively immature flies throughout the year was observed at San Diego, where the highest percentage of mated, gravid flies was present in June, July and August (fig. 5E). The proportion of reproductively immature flies increased in spring or early summer at all locations, a period during which the European literature suggests that a reproductive diapause may occur. However, reproductively mature flies were also present at this time. A decrease in mean egg load was observed during the spring and fall (data not shown). At no point during the summer months were reproductively mature females completely absent. Egg load was positively related to mating status (F1, 3049 = 160.20, P < 0.0001) at all locations for all months. Mean egg load was larger in mated than unmated flies, regardless of month, and was greatest in March and May and least in September. On average, mated flies had 7.30 eggs in their ovaries, while unmated flies had 2.44 eggs present. Flies with mature eggs in their ovaries were more likely to be mated (2 = 1228.4922, df = 1, P < 0.0001). Population densities as indicated by trap captures were high at both the Butte and San Diego sites (table 2) relative to the other sites. McPhail traps are thought to overestimate the proportion of gravid female flies in a population (Neuenschwander and Michelakis 1979), so the abundance of reproductively immature flies is likely not due to greater trap capture and it is
possible that the proportion of immature flies may be even greater than that observed through trap captures. The climate at San Diego is characterized
by moderate, coastal-influenced temperatures throughout the year, as opposed to hot summer and relatively cool winter temperatures that fall below
(A) Yolo 1 (n = 1,133)

100 80 60 40 20 0 100 80 60 40 20 0 100 bc c a abc ab a ab bc bc abc c a ab abc bc c c c Mar bcd Apr ab May d June cd July bcd Aug bc Sep ab Oct a Nov a
(B) Solano 4 (n = 972)

ab a bc bc b c b ab a
(C) Butte 1 (n = 870)

a a cd cd d ab bc a ab
Dissected females (%)
80 60 40 20 0 100 80 60 40 20 0 100 80 60 40 20 0 ab Mar ab Apr a May b June b July b Aug ab Sep ab Oct a Nov abc bc c a abc bc c ab ab bc c a a a bc b bc bc
(D) Napa 1 (n = 937)

bcd abc a d d abcd ab cd cd
(E) San Diego 1 (n = 1,095)

bc bc bc ab a ab bc bc c
Collection month
Unmated, immature Unmated, mature Mated, immature Mated, mature
Fig. 5. Ovarian development and mating status for olive fruit fly at five locations. Flies were categorized as (1) unmated (sperm absent), immature ovaries, (2) unmated, mature ovaries, (3) mated (sperm present), immature ovaries and (4) mature, mature ovaries. Only flies in category (4) would be capable of infesting olives. Flies were collected weekly, and data pooled by month. Percentages of a given class (unmated/immature or mated/mature) indicated by the same letter for a single location were not significantly different ( = 0.05) when adjusted means were compared via LSD; data from December, January and February was eliminated from analysis for all years due to insufficient sample sizes.
the fruit fly development thresholds. Therefore, more-extensive generational overlap might be expected at the San Diego site than at the Butte site, resulting in more young, reproductively immature females present in the population year-round.
Managing olive fruit fly
UC researchers have developed a greater understanding of the behavior and biology of the olive fruit fly in the 12 years since its initial detection, but there is still a great deal of work to be
done to develop tools to apply this information in effectively managing this pest. Models determining when olives become susceptible to olive fruit fly attack and how fly populations respond to climatic conditions are being developed using the data described here. With a few exceptions, the olive fruit fly has not prevented commercial olive production in California for most growers, but it has significantly changed their insect management requirements.
Statewide surveys have gathered important information about the life cycle of the olive fruit fly, which will be used to improve pest management practices. Above, larvae infest olive fruit.
H.J. Burrack is Assistant Professor of Entomology, North Carolina State University, Raleigh; R. Bingham is Entomologist, Plant Industry, California Department of Food and Agriculture; R. Price is Agricultural Commissioner, Butte County; J.H. Connell is Farm Advisor, UC Cooperative Extension (UCCE) Butte County; P.A. Phillips is Regional IPM Farm Advisor, retired; L. Wunderlich is Farm Advisor, UCCE Amador and El Dorado counties; P.M. Vossen is Farm Advisor, UCCE Sonoma and Marin counties; N.V. OConnell is Farm Advisor, UCCE Tulare County; L. Ferguson is Professor of Plant Sciences, UC Davis; and F.G. Zalom is Professor of Entomology, UC Davis. The authors would like to thank 19 trappers for collecting data from 28 locations in 16 counties over the course of 4 years.
References
Augustinos AA, Stratikopoulos EE, Zacharopoulou A, Mathiopoulos KD. 2002. Polymorphic microsatellite markers in the olive fly, Bactrocera oleae. Mol Ecol Notes 2:27880. Burrack HJ. 2007. The Seasonal Biology of the Olive Fruit Fly in California. Ph.D. dissertation, UC Davis. 123 p. Burrack HJ, Connell JH, Zalom FG. 2008. Comparison of olive fruit fly (Bactrocera oleae [Rossi]) (Diptera: Tephritidae) captures in several commercial traps in California. Int J Pest Manag 54(3):22734. Burrack HJ, Zalom FG. 2008. Oviposition preference and larval performance of the olive fruit fly (Diptera: Tephritidae) in several commercially important olive varieties in California. J Econ Entomol 101(3):7508. Collier TR, Van Steenwyk RA. 2003. Prospects for integrated control of olive fruit fly are promising in California. Cal Ag 57:2831. Connell JH. 2005. History and scope of the olive industry. In: Sibbett GS, Ferguson L (eds.). Olive Production Manual (2nd ed.). UC ANR Pub 3353. Oakland, CA. p 110. Daane KM, Rice RE, Zalom FG, et al. 2005. Arthropod pests of olive. In: Sibbett GS, Ferguson L (eds.). Olive Production Manual (2nd ed.). UC ANR Pub 3353. Oakland, CA. p 10514. Delrio G, Prota R. 1976. Osservaziono eco-etologiche sul Dacus oleae Rossi nella Sardegna nord-occidentale. Boll Zool Agrar Bachi 2:49118.
Economopoulos AP, Haniotakis GE, Michelakis S, et al. 1982. Population studies on the olive fruit fly, Dacus oleae (Gmel.) (Dipt., Tephritidae) in Western Crete. Z Entomol 93:46376. Fletcher BS, Pappas S, Kapatos E. 1978. Changes in the ovaries of olive flies (Dacus oleae [Gmelin]) during the summer, and their relationship to temperature, humidity and fruit availability. Ecol Entomol 3:99107. Fritz AH, Turner FR. 2002. A light and electron microscopical study of the spermathecae and ventral receptacle of Anastrepha suspensa (Diptera: Tephritidae) and implications in female influence of sperm storage. Arth Struc Dev 30:293313. Kicenik Devarenne A, Vossen PM. 2007. Monitoring and organic control of olive fruit fly. In: Vossen PM (ed.). Organic Olive Production Manual. UC ANR Pub 3505. Oakland, CA. p 4751. Koveos DS, Broufas GD, Kiliaraki EK, Tzanakakis ME. 1997. Effect of prevention of flight on ovarian maturation and reproductive diapause in the olive fruit fly (Diptera: Tephritidae). Ann Entomol Soc Am 90:33740. Koveos DS, Tzanakakis ME. 1990. Effect of the presence of olive fruit on ovarian maturation in the olive fruit fly, Dacus oleae, under laboratory conditions. Entomol Exp Appl 55:1618. Koveos DS, Tzanakakis ME. 1993. Diapause aversion in the adult olive fruit fly through effects of the host fruit, bacteria and adult diet. Ann Entomol Soc Am 86:66873. Nardi F, Carapelli A, Dallai R, Roderick GK. 2005. Population structure and colonization history of the olive fly, Bactrocera oleae (Diptera, Tephritidae). Mol Ecol 14:272938.
Neuenschwander P, Michelakis S. 1979. McPhail trap captures of Dacus oleae (Gmel.) (Diptera, Tephritidae) in comparison to the fly density and population composition as assessed by sondage in Crete, Greece. Mitt Schweiz Entomol Ges 52:34357. Raspi A, Canale A, Loni A. 2005. Presence of mature eggs in olive fruit fly, Bactrocera oleae (Diptera Tephritidae), at different constant photoperiods and at two temperatures. Bull Insectol 58:1259. Raspi A, Iacono E, Canale A. 2002. Variable photoperiod and presence of mature eggs in olive fruit fly, Bactrocera oleae (Rossi) (Diptera Tephritidae). Redia 85:1119. Rice RE, Phillips PA, Stewart-Leslie J, Sibbett GS. 2003. Olive fruit fly populations measured in Central and Southern California. Cal Ag 57(4):1227. Tzanakakis ME. 1986. Summer diapause in the olive fruit fly and its significance. Int Symp Fruit Flies of Economic Importance, Crete. p 3836. Vossen PM. 2007. Olive oil: History, production and characteristics of the worlds classic oils. HortScience 42(5):1093100. Wang X-G, Johnson MW, Daane KM, Nadel H. 2009. High summer temperatures affect the survival and reproduction of olive fruit fly (Diptera: Tephritidae). Env Entomol 38(5):1496504. Yokoyama VY, Miller GT, Stewart-Leslie J, et al. 2006. Olive fruit fly (Diptera: Tephritidae) populations in relation to region, trap type, season and availability of fruit. J Econ Entomol 99(6):20729.
20
REVIEW ARTICLE
Biological controls investigated to aid management of olive fruit fly in California

by Kent M. Daane, Marshall W. Johnson, Charles H. Pickett, Karen R. Sime, Xin-Geng Wang, Hannah Nadel, John W. Andrews Jr. and Kim A. Hoelmer
The widespread and rapid establish ment of the olive fruit fly in Califor nia required immediate changes in integrated pest management (IPM) programs for olives. After find ing that resident natural enemies did not provide adequate control, researchers began a worldwide search for parasitoids, with explora tion in the Republic of South Africa, Namibia, India, China and other countries. Parasitoids were shipped to California, and most were studied in quarantine to determine the best which serve as reservoirs and contribute to the flys reinvasion of treated orchards (Collier and Van Steenwyk species for release. Two parasitoid 2003). Classical biological control the species Psyttalia lounsburyi and importation of natural enemies from Psyttalia humilis are now be the pests home range offers the best ing released throughout the states opportunity to economically suppress olivegrowing regions, and research olive fruit fly populations in these situations. We review ongoing efforts in ers are studying their effectiveness. California to (1) document the natural enemies of olive fruit fly already present, (2) search for and import novel he olive fruit fly was first found in natural enemies from other countries Southern California in 1998 (Rice et and (3) determine the effectiveness al. 2003). Facilitated by longevity and and limitations of these natural enemy the adults ability to fly long distances, species. To date, California scientists the fly dispersed rapidly throughout the have received approval from the U.S. state. There was little opportunity to at- Department of Agricultures Animal tempt a statewide eradication program, and Plant Health Inspection Service so current research efforts emphasize (USDA-APHIS) for the release of sevlong-term management practices. Bioeral parasitoid species, and permits are logical control may be a part of this pro- pending for two others (see page 26). gram (Daane and Johnson 2010). Natural enemies in California How might natural enemies conAlthough the olive fruit fly is native tribute to the control of olive fruit fly to Africa and Asia (Nardi et al. 2005), (Bactrocera oleae [Rossi])? Commercial some North American predators and orchards now rely upon a broadparasitoids may attack it. Insect predaspectrum insecticide combined with tors such as lady beetles and lacewings a highly attractive bait (Johnson et al. are found in olive orchards, but because 2006). The effectiveness of insecticidethe flys eggs are embedded underneath based programs is, however, limited the fruits epidermis and the larvae feed by the abundance of roadside and deep inside the fruit (Tzanakakis 2006), residential olive trees in California, the immature stages are protected from most generalist predators. Before the larva pupates, it creates a thin window on the fruit surface through which it may be exposed to predators. If the fruit is still firm, the larva will often pupate inside. However, upon fruit maturation most fly larvae leave the older fruit, especially in the late summer and fall, and drop to the ground to pupate in the soil beneath the tree (Tzanakakis 2006). Orsini et al. (2007) placed fly puparia (which enclose the fly pupa) on the ground in olive orchards and used different barriers around each to distinguish mortality levels due to abiotic (e.g., climate) and biotic (e.g., predators) factors. In an August trial, olive fruit fly exposed to predators was reduced by about 60% compared to other treatments (fig. 1). Ants (e.g., Formica species) were the most abundant predators on the ground and were observed carrying and killing olive fruit fly pupae. Predation rates vary among orchards, depending on factors such as the species and densities of predators present and the soil depth at which fly pupae are located. European studies similarly indicate that arthropods can inflict substantial mortality on olive fruit fly pupae (Daane and Johnson 2010; Tzanakakis 2006).
Parasitoids imported into California for quarantine studies include braconid parasitoids reared from wild olive fruit fly, (A) Psyttalia lounsburyi, (B) Bracon celer and (C) Utetes africanus, as well as braconid parasitoids reared on other fruit fly species, including (D) Diachasmimorpha longicaudata, (E) D. kraussii and (F) Fopius arisanus.
A California-resident parasitoid has also been found attacking olive fruit fly. The parasitoid is similar to the European Pteromalus myopitae (Graham) (Hymenoptera: Pteromalidae), hence it is currently referred to as Pteromalus species near myopitae (P. sp. nr. myopitae). It has been reared from olive fruit fly collected primarily in coastal counties from San Luis Obispo to San Diego, although it has also been collected in Alameda, Butte, Fresno, Solano and Yolo counties. This parasitoid is solitary (one per fly larva) and feeds externally on third-instar olive fruit fly. An olive fruit fly survey in San Luis Obispo County reported an average parasitism level of 2.98% by P. sp. nr. myopitae (Kapaun et al. 2010). Parasitism levels varied considerably, ranging from 0% to 33% (based on collections of 100 infested fruit per week) with activity highest in August and September. Because P. sp. nr. myopitae has never been reported elsewhere, it is likely a North American parasitoid of native fruit flies; it opportunistically parasitizes olive fruit fly but has never been collected on any native fruit fly species despite numerous surveys.
Foreign exploration
Imported material. Resident natural enemies do not adequately suppress olive fruit fly populations below damaging levels. For this reason, California researchers began seeking natural enemies abroad in 2003. The
Olive fruit y pupae recovered (% SEM)
Pteromalus species near myopitae is resident to California and has been reared from olive fruit fly collected primarily in coastal counties. The adult (A) oviposits onto second- or third-instar fly larvae, placing an egg (B) on the outside of the larva, where the parasitoid larva (C) develops as a solitary, external parasitoid.
100 80 60 40 20 0
Laboratory control
Total exclusion
Predator exclusion
Exposed
Fig. 1. Mean percentage ( SEM) of olive fruit fly pupae recovered after 4 days (August 2005) when held in laboratory control, and placed in an olive orchard where treatments were total exclusion of all natural enemies; predator exclusion, preventing walking predators from reaching pupae; and exposed, allowing both flying and walking natural enemies access to pupae. Different letters above each bar indicate significant differences (Tukeys HSD test, P < 0.05) (Orsini et al. 2007).
search started in Africa, where olive fruit fly probably originated and there is a rich diversity of fruit fly parasitoids. Olive fruit fly parasitoids were reported in Africa as early as 1912 by the renowned Italian entomologist Filippo Silvestri during surveys for parasitoids of Mediterranean fruit fly (Medfly) (Ceratitis capitata [Wiedemann]) (Wharton 1989). Members of the USDA Agricultural Research Services European Biological Control Laboratory, the California Department of Food and Agriculture, UC researchers and cooperators explored the Republic of South Africa, Namibia, Kenya, La Runion (an island east of Madagascar), the Canary Islands, Morocco, Pakistan, India and China. Collections for specialists (i.e., natural enemies that primarily attack one species) were made from wild olive fruit (Olea europaea ssp. cuspidata) from south to northeast Africa, and from southwest Asia to central China. The parasitoids reared from olive fruit fly included Psyttalia lounsburyi (Silvestri), Psyttalia concolor (Szpligeti), Psyttalia humilis (Szpligeti), Psyttalia ponerophaga (Silvestri), Utetes africanus (Silvestri) and Bracon celer Szpligeti. The greatest yield of parasitoids came from collections made in South Africa, Namibia and Kenya (table 1). The most common species were U. africanus, P. lounsburyi and P. humilis (table 1). The highest levels of parasitism were found in Kenya collections where P. lounsburyi and U. africanus together parasitized more than 57% of collected flies. The next highest parasitism levels were in collections from Pakistan (27.7% parasitism by P. ponerophaga) and Republic of South Africa (27.8% to 68.0% parasitism by P. humilis, P. lounsburyi, B. celer and U. africanus during 3 years
of collections). Although P. concolor was the only olive fruit fly parasitoid found in Morocco and the Canary Islands, parasitism rates were limited to 14.6% and 2.3%, respectively. Similarly, in the Republic of South Africa, P. humilis accounted for less than 4% of parasitism. However, in Namibia P. humilis was the dominant parasitoid and attained parasitism levels from 18.1% to 35.1%. In China, few olive fruit flies were collected, although one (unidentified) Diachasmimorpha species was obtained, and in India no olive fruit were found on wild olive trees during the 2006 and 2007 explorations (Alan Kirk, personal communication). Numerous fruit fly parasitoids are known to attack other flies in the genus Bactrocera. A few of these more generalist parasitoids (i.e., natural enemies that attack numerous species) were also imported to California. These were Fopius arisanus (Sonan), Diachasmimorpha kraussii (Fullaway) and D. longicaudata (Ashmead). All were supplied by Russell Messing at University of Hawaii, where they had been reared on Medfly. Similarly, colonies of P. humilis maintained on Medfly in Guatemala were sent to California, supplied by Pedro Rendon of the USDA APHIS Plant Protection and Quarantine program (Yokoyama et al. 2008, 2010). Reported efforts. A parasitoids performance in other regions provides insights for researchers when determining which natural enemy species should be released. P. lounsburyi was identified nearly 100 years ago as an olive fruit fly parasitoid and is often reported as the most effective natural enemy in wild olives of southern Africa (Copeland et al. 2004). P. ponerophaga has a similar long association with olive fruit fly and is the only olive fruit fly specialist
22
known from Pakistan (Wharton 1989). was introduced to the Hawaiian Islands Johnson 2010). Diachasmimorpha kraussii However, no systematic effort has been in the 1940s and provided excellent is native to Australia, attacks a range of made to include these parasitoids in control of Oriental fruit fly (Bactrocera Bactrocera species and has been released European biological control (Wharton dorsalis [Hendel]). It now also contribin Hawaii to control Medfly (Bokonon1989), presumably because they have utes to Medfly control (Wang, Messing, Ganta et al. 2007); we have found no been difficult to import and rear. Bautista, et al. 2003). Following the reports of its use against olive fruit fly, We found no reports of concerted success in Hawaii, F. arisanus was intro- but it has been reported attacking olive efforts to import or manipulate U. afduced widely to control these and other fruit fly in Israel (C.H. Pickett, personal ricanus for biological control, although tephritid pests in Australia, Central communication). in some South African surveys it is an America, various Pacific and Indian Quarantine nontarget studies abundant olive fruit fly parasitoid in Ocean islands, and the Mediterranean Before exotic natural enemies are wild olives (Hancock 1989). Similarly, Basin, though not all of these introducreleased in California, quarantine studB. celer is often the most commonly retions have been as effective. The few ported parasitoid attacking olive fruit attempts to establish F. arisanus on olive ies are conducted to determine whether or not they will attack insect species fly in commercial and wild olives in fruit fly in Europe were unsuccessful. other than the intended target (Hoelmer South Africa (Neuenschwander 1982), One study reported that F. arisanus and Kirk 2005). There are more than where it achieved parasitism rates as failed to reproduce on olive fruit fly 140 tephritids in California (Foote et al. high as 87%. However, small-scale atin field cages (Neuenschwander et al. 1993), including some endemic species tempts to rear and/or release B. celer 1983); however, more recent laboratory in Europe have been unsuccessful work has confirmed that F. arisanus can and others that were brought into the state for the biological control of weeds. (Wharton 1989). reproduce on olive fruit fly (Calvitti et Rather than test all of these species, Instead, biological control of olive al. 2002; Sime et al. 2008). fruit fly has focused on members of the D. longicaudata, a native of Southeast researchers assess parasitoid responses P. concolor species complex, which inAsia (Wharton 1989), attacks a relatively to fruit fly species found in the three common habitats of fruit fly larvae cludes P. concolor from northern Africa wide range of tephritid flies, including fruits, flower heads and stem galls to and P. humilis from sub-Saharan Africa, Medfly, Oriental fruit fly, Caribbean explore their tendency to specialize on especially after an efficient massfruit fly (Anastrepha suspensa [Loew]) rearing method was developed in the and Mexican fruit fly (A. ludens [Loew]) certain host habitats. Tested species are selected to maximize both practicality 1950s using Medfly reared on an arti(Wang and Messing 2004). It has been (ease of locating and/or rearing hosts) ficial diet (Daane and Johnson 2010). used widely for biological control. One and potential for host acceptance (reHowever, P. concolor has not provided attempt was made to rear and release semblance of infested plant structure to adequate or consistent olive fruit fly it against olive fruit fly in Greece, but it control in Europe and, where it has esdid not become established (Daane and olives in shape or size). Therefore, most tablished, repeated mass releases are required to boost TABLE 1. Fruit fly and parasitoids reared from field-collected wild olives for importation into California, 20032007 parasitism rates (Copeland et al. 2004). Nonetheless, we Species reared* consider P. concolor and P. Diachas humilis to be important to Insects Bactrocera Psyttalia Psyttalia Psyttalia Psyttalia Utetes Bracon mimorpha screen for use in California Country Year reared spp. humilis concolor lounsburyi ponerophaga africanus celer spp. biological control. Their na....................................%..................................... n tive range spans much of Morocco 2004 318 85.4 0.0 14.6 0.0 0.0 0.0 0.0 0.0 northern and eastern Africa 2004 965 97.7 0.0 2.3 0.0 0.0 0.0 0.0 0.0 (Wharton and Gilstrap 1983) Canary Islands and, given the diversity of Pakistan 2005 636 72.3 0.0 0.0 0.0 27.7 0.0 0.0 0.0 habitats and climates enLa Runion 2004 700 86.0 0.0 0.0 0.0 0.0 0.0 0.0 14.0 compassed, they likely comNamibia 2004 597 69.2 18.1 0.0 0.0 0.0 3.7 9.0 0.0 prise several biotypes, or 2007 874 58.1 31.3 0.0 9.0 0.0 1.6 0.0 0.0 even new species or geneti2008 3,077 50.0 35.1 0.0 11.0 0.0 3.3 0.6 0.0 cally differentiated populaSouth Africa 2003 2,218 49.5 3.2 0.0 14.9 0.0 22.8 9.6 0.0 tions (Rugman-Jones et al. 2004 794 32.2 2.2 0.0 14.3 0.0 46.1 5.2 0.0 2009), some of which may 2005 377 72.2 0.0 0.0 15.1 0.0 12.7 0.0 0.0 be better suited to control Kenya 2005 3,647 42.5 0.0 0.0 35.6 0.0 21.9 0.0 0.0 olive fruit fly in California China 2007 438 97.5 0.0 0.0 0.0 0.0 0.0 0.0 2.5 (Yokoyama et al. 2010). F. arisanus is well known India 2006 0 as a generalist parasitoid of 2007 0 fruit-infesting tephritids. * Percentages of adult olive fruit fly and parasitoids reared are shown; does not include gall-formers or unknown parasitoid species that may have been reared from galls, from other fruit fly species or as hyperparasitoids on primary parasitoids of olive fruit fly. Native to Southeast Asia, it
of the imported parasitoids were either sent directly to the UC Berkeley quarantine facility, or to the collaborating laboratory in France and then to the UC Berkeley facility. Olive fruit fly belongs to the tephritid subfamily Dacinae, which is not native to North America. Californias native and introduced fruit fly species fall into two other subfamilies, Trypetinae and Tephritinae (Foote et al. 1993). For a nontarget, fruit-feeding Trypetinae, researchers selected the native black cherry fly (Rhagoletis fausta [Osten Sacken]), which infests fruit of bitter cherry. For a flower-head feeder, they selected Chaetorellia succinea (Costa), an imported Tephritinae used to control yellow starthistle (Centaurea soltitialis L.). For a gall-former, researchers selected another Tephritinae biological control agent, Parafreutreta regalis (Munro), which forms stem galls in Cape ivy. The testing of C. succinea and P. regalis addressed the risk posed to beneficial species by the candidate parasitoids. Unless stated otherwise, these three species were common to all UC Berkeley quarantine studies; other nontarget fruit flies were tested when available. There was some variation in the materials and methods used to test the different species, but procedures were generally as described by Daane et al. (2008). Briefly, researchers used
were limited to the weed biologicalcontrol agents C. succinea (yellow starthistle fly) and P. regalis (Cape ivy fly) and no fruit-infesting fly species were tested. In no-choice tests, P. ponerophaga adults probed into galls on Cape ivy and produced parasitoid offspring from this nontarget host, but did not probe or reproduce in yellow starthistle (table 2). P. concolor and P. humilis. P. concolor should be viewed as a species complex, as previously mentioned. While similar, there may be biological differences that influence their affectiveness in California. For example, researchers Parasitoids and olive fruit fly found that even P. humilis colonies from P. lounsburyi. P. lounsburyi was the different locations had slightly differonly parasitoid tested that probed only ent levels of host specificity (table 2). into infested olives and reproduced However, P. concolor and P. humilis popsolely on olive fruit fly (table 2). That ulations tested were able to reproduce P. lounsburyi is relatively specialized on on nontarget Cape ivy fly. In other laboolive fruit fly is supported by the fact ratory studies, P. concolor was similarly that it had been reared only from olive reared from numerous fruit fly species fruit fly in decades of field collections of (Wharton and Gilstrap 1983). However, African fruit flies (Copeland et al. 2004; small-cage trials are artificial, and olive Wharton et al. 2000). In addition, its fruit fly and Medfly are the primary geographic range is entirely contained hosts of P. concolor and P. humilis in their within that of olive fruit fly. native African range (Copeland et al. P. ponerophaga. It has been sug2004; Wharton et al. 2000). B. celer. B. celer also attacked gested that P. ponerophaga specializes and reproduced on Cape ivy fly, but on olive fruit fly because the parasitoid surprisingly did not reproduce on the has only been reported from this speblack cherry fly, the fruit-infesting cies (Sime et al. 2007). Quarantinescreening studies of nontarget impacts fly tested with this species (table 2). However, B. celer did probe on host materials for all fruit flies presented except TABLE 2. Host-specificity trials searching, probing and reproduction by imported parasitoids currant fly. To date, B. celer has been on olive fruit fly and nontarget fruit fly species reported only as a parasitoid of olive fruit fly and Medfly in field surveys Yellow Olive Cherry Apple Cape starthistle Currant (Wharton et al. 2000), with an addiParasitoids* fruit fly fly maggot ivy fly fly fly Reference tional, unconfirmed record on Ceratitis Psyttalia concolor (Italy) S/P/R S/P S/P S/P/R S/P NI Unpublished data nigra Graham. Psyttalia humilis (Kenya) S/P/R S/P S/P S/P/R NI S Unpublished data U. africanus. One of the most comPsyttalia humilis (Namibia) S/P/R S/P/R NI Unpublished data monly recovered species in the South Psyttalia unknown sp. A S/P/R S/R NI S/P/R NI NI Unpublished data African collections, U. africanus was Psyttalia ponerophaga S/P/R S/P/R NI Unpublished data difficult to rear in quarantine. It reproPsyttalia lounsburyi S/P/R NI NI S NI NI Daane et al. 2008 duced on olive fruit fly, as expected, Diachasmimorpha S/P/R S/P/R S/P S/P/R NI NI Unpublished data but this parasitoid was never observed longicaudata to show any interest (by searching or Diachasmimorpha kraussii S/P/R S/P/R S S/P/R S/P/R S/P Unpublished data probing) in either the target or nontarBracon celer S/P/R S/P NI S/P/R S/P NI Nadel et al. 2009 get host plants during tests (table 2). Utetes africanus R NI NI NI Unpublished data The literature indicates that U. africanus Fopius arisanus S/P/R NI NI Sime et al. 2008 has been reared from olive fruit fly, * Target host was olive fruit fly; nontarget hosts were cherry fly (Rhagoletis fausta [Osten Sacken]), apple maggot (Rhagoletis Medfly, Oriental fruit fly, coffee fruit pomonella [Walsh]), Cape ivy fly (Parafreutreta regalis [Munro]), yellow starthistle fly (Chaetorellia succinea [Costa]) and fly (Trirhithrum coffeae Bezzi) and natal currant fly (Euphranta canadensis [Loew]). S = host plant searched by parasitoid; P = host plant probed by parasitoid; R = parasitoid successfully reproduced in host; fly (Ceratitis rosa Karsch) (Wharton and NI = parasitoid showed no interest in host plant or host during observation period; = not tested. Gilstrap 1983). small cages (about 12 square inches) to isolate female parasitoids with either target (olive fruit fly) or nontarget hosts for 48 hours in a no-choice test. Target and individual nontarget species were then placed together for a choice test for the next 48 hours. The number of searching events (i.e., parasitoids on the host plant) and probing events (i.e., parasitoids inserting their ovipositor to place an egg into the fruit, flower head or gall) were recorded during discrete observation periods. Afterward, the host material was isolated and held for parasitoid or fly emergence.
24
Diachasmimorpha species. D. longicaudata and D. krausii were the most aggressive of the quarantine-screened parasitoids, probing nearly all host material presented and producing offspring from nontarget, fruit-infesting species as well as the beneficial species (table 2). This result was not surprising because in total they have been reared from more than 20 fruit fly species (Wharton and Gilstrap 1983). F. arisanus. While F. arisanus is considered more of a generalist, it is not attracted to either C. succinea eggs on yellow starthistle buds, or P. regalis eggs in Cape ivy stems or the associated galls (table 2). These results are consistent with studies in Hawaii that show F. arisanus only attacking fruitfeeding tephritids (Wang, BokononGanta, et al. 2004). The host range in F. arisanus is probably constrained by its host-searching behavior: females are generally stimulated to search for host eggs by fruit odors; smooth, round fruit surfaces; and oviposition punctures left by flies (Wang and Messing 2003). Introducing F. arisanus to California still requires evidence that native, fruitfeeding Tephritidae are unlikely to be attacked. Sixteen tephritid species native to California feed in fruit (Foote et al. 1993), but at least eight are found at higher elevations where F. arisanus, a tropical species, is unlikely to flourish.
Parasitoid biology studies
Researchers studied the biology of imported natural enemies to help
determine the best combination of species for release in Californias climatically varied olive-growing regions. Parasitoid host-stage preference, development time, adult longevity and fecundity (offspring per female) were determined when colony numbers permitted these additional quarantine studies (table 3). Host-stage preference. Newly infested olives were held for different lengths of time to create fruit with various olive fruit fly host age categories (i.e., different immature fly stages). These infested olives were placed with mated female parasitoids, and the amount of time the parasitoids searched and probed on the different age categories was recorded. After the exposure period, the olives were held to rear either adult parasitoids or flies. These experiments established that P. lounsburyi, P. ponerophaga, P. concolor, P. humilis, D. longicaudata and D. kraussii were internal parasitoids that preferred to oviposit into second- or third-instar olive fruit fly (table 3). B. celer is an external-feeding parasitoid that prefers late third-instar maggots. F. arisanus is an egg-larval parasitoid that inserts its eggs into olive fruit fly eggs, and the parasitoid completes its life cycle in the larval olive fruit fly. F. arisanus females may sometimes lay their eggs in firstinstar olive fruit fly. Host-stage preference did not always correlate with reproductive success. This was most clearly seen in trials with P. lounsburyi, where adults spent
more time probing olives with larger third-instar maggots (fig. 2A), but more offspring were produced from olives containing smaller second- and thirdinstar maggots (fig. 2B). Many parasitoids locate hidden hosts by detecting substrate vibrations. For example, adult P. concolor are thought to respond more
8
(A) Parasitoids Observed on olives

6 ab
4 a
Egg1st 1st2nd 2nd3rd
3rd
Late 3rd
50
(B) Adult offspring

40
b b
Emergence (%)
30 20 10 0 a
b ab
Egg1st 1st2nd 2nd3rd
3rd
Late 3rd
Host stage (instar)
Fig. 2. Host-stage preference as mean percentage ( SEM) of (A) adult female Psyttalia lounsburyi on olives containing hosts of a given age category during timed observations and (B) P. lounsburyi offspring that emerged from different host-stage categories. Different letters above each bar indicate significant differences (one-way ANOVA, P < 0.05) (Daane et al. 2008).
TABLE 3. Key biological parameters for parasitoids of olive fruit fly studied in UC Berkeley quarantine facility Development time (egg to adult) Offspring per female n 10.2 2.6 18.7 2.9 22.5 5.1 28.7 4.1 35.2 4.1 48.8 8.5 9.7 7.2 23.6 5.3 22.7 5.5 4.4 0.8 Daane et al. 2008 Sime et al. 2007 Sime, Daane, Messing, et al. 2006 Sime, Daane, Messing, et al. 2006 Daane/Sime, unpublished data Daane/Sime, unpublished data Sime, Daane, Andrews et al. 2006 Daane/Sime, unpublished data Sime, Daane, Nadel, et al. 2006 Sime, Daane, Nadel, et al. 2006 Sime et al. 2008
Parasitoid species tested
Host-stage preference
Adult longevity
Reference
. . . . . . . . . . . . . . days . . . . . . . . . . . . . . P. lounsburyi P. ponerophaga P. concolor (Italy) P. humilis (Kenya) P. humilis (Namibia) P. concolor (South Africa) B. celer U. africanus D. longicaudata D. kraussii F. arisanus Second to third instar Second to third instar Second to third instar Second to third instar Second to third instar Second to third instar Third instar Second to third instar* Second to third instar Second to third instar Egg 22.8 0.8 (75F) 20.5 1.5 (77F) 16.4 0.6 (77F) 18.1 0.4 (77F) 35.5 0.8 (72F) 20.5 1.0 (75F) 20.8 0.9 (77F) 21.6 1.7 (77F) 61.8 8.2 36.2 4.9 68.8 16.4 77.6 15.3 36.0 7.3 53.2 6.6 51.0 11.7 59.2 5.0 64.1 7.8
*Few replicates were completed with U. africanus, and only 10 adults were reared from olive fruit fly during the trial.
80
a a D. kraussii D. longicaudata
Mean longevity (days)
60
40 b 20 c 0 c Nothing
Honey water
Olives/ honey water
Hosts/ honey water
Water
Fig. 3. Adult female Dichasmimorpha kraussii and D. longicaudata longevity given different food provisions. Different letters above each bar indicate significant treatment differences (Tukeys HSD test, P < 0.05) (Sime, Daane, Nadel, et al. 2006).
strongly to the third than the second instar because the larger instar produces stronger or more frequent vibrations while feeding (Canale and Loni 2006). However, the third-instar olive fruit fly maggots feed deeper in olives and may be beyond the reach of the short P. lounsburyi ovipositor (less than 2 millimeters). Development time. The egg-to-adult developmental rates of P. lounsburyi, P. ponerophaga, P. concolor, D. kraussii and D. longicaudata were relatively similar, about 22 days at constant temperatures near 77F (25C), while B. celer required nearly 40% more time (table 3). Olive fruit fly requires about 23 days at 77F (25C), suggesting that (except for B. celer) these parasitoids could have generation times similar to olive fruit fly. Adult longevity. When provisioned with water and honey, examined adult parasitoid species lived 36 to 78 days at temperatures around 77F (25C) (table 3). For all tested species, adults lived for less than 5 days without food, as shown for D. longicaudata and D. kraussii (fig. 3). For most species studied, there was also a reduction in longevity when adults were provided hosts in infested olives, suggesting that the parasitoids expended energy while handling hosts and that the parasitoids were able to distinguish host-infested olives from those lacking hosts. Tolerances for high and low temperatures may be critical for parasitoid establishment in California because olive fruit fly infestations are found in both
26
relatively cool coastal and hot inland areas, resulting in different seasonal development of the fly (Yokoyama et al. 2006). Overall patterns of adult longevity for all parasitoids tested showed a negative correlation with temperature, as shown for the Kenya and Italy colonies of P. humilis (fig. 4). Lifetime fecundity. Researchers studied the parasitoids reproductive potential by providing newly emerged and mated adult females with an overabundance of infested olives every 2 days (table 3). All species tested deposited most of their eggs during the first third or half of their life span (fig. 5). Surprisingly, the two specialists (P. lounsburyi and P. ponerophaga) had the lowest lifetime fecundity of the larval endoparasitoids, which develop inside the host (table 3). One hypothesis to explain these low fecundity rates concerns the relative lengths of their ovipositors (see below). Another explanation concerns the chemical cues used to orient to and identify host larvae and the host/plant complex. Domestic olives differ chemically from wild olives. These differences could disrupt the parasitoids host-searching, hostidentification or ovipositional behaviors, or impede larval development. Quarantine studies also reported low lifetime fecundity for B. celer, the external parasitoid, and F. arisanus, the egg-larval parasitoid (table 3), although in each case researchers suggest that experimental conditions may have negatively influenced natural egg deposition. In the UC Berkeley quarantine studies, researchers found up to 80% mortality of olive fruit fly eggs exposed to F. arisanus (Sime et al. 2008). Similar findings have previously been reported on olive fruit fly (Calvitti et al. 2002) and other hosts (Moretti and Calvitti 2003). Most likely this direct mortality results from the egg being repeatedly probed (i.e., stabbed) by the F. arisanus ovipositor. Olive fruit fly lays a single egg per fruit puncture, whereas the typical host of F. arisanus, the Oriental fruit fly, deposits up to 100 eggs per puncture (Ramadan et al. 1992). The tendency of F. arisanus to probe repeatedly within an oviposition puncture may be an evolutionary consequence of its use of this host. By comparison, more than 100 progeny can be obtained
per female F. arisanus when reared on the Oriental fruit fly (Ramadan et al. 1992).
Releasing natural enemies
California researchers received USDA-APHIS approval for the release of P. lounsburyi and limited release of P. humilis; approval is pending for P. ponerophaga; and permits for the limited release of F. arisanus are being prepared. To date, P. lounsburyi has been released and recovered in field-cage studies, but has not yet been shown to overwinter. More work has been done with P. humilis, which is easier to rear, and levels of up to 60% parasitism have been reported from cage studies (Wang, Johnson, Daane, Yokoyama 2009; Yokoyama et al. 2008, 2010). However, as with P. lounsburyi, there is no clear evidence to date that P. humilis can
120 100 80 60 40 20 0 50 Kenya, female Kenya, male Italy, female Italy, male
Adult longevity (days)
59
68
77
86
95
Temperature (F)
Fig. 4. Adult P. humilis longevity declined with increasing constant temperature for each gender and culture. Within each culture, no significant differences were found between female and male longevity at any temperature tested (Sime, Daane, Messing, et al. 2006).
10 8 6 4 2 0 0 10 20 30 40 50
Offspring per female
Time (days)
Fig. 5. Mean lifetime production of offspring ( SEM) produced by P. humilis from a Kenyan culture (Sime, Daane, Messing, et al. 2006).
establish and thrive without repeated augmentation. There is a risk with the release of each natural enemy species that some nontarget species will be attacked, but the benefits often outweigh the risks (Hoddle 2004). Also, not all pest species are prime targets for classical biological control there are potential problems with olive fruit fly and natural enemy biology that may limit the levels of control achieved. Seasonal host availability. The olive fruit flys survival is limited in regions with high or low temperature extremes (Wang, Johnson, Daane, Opp 2009). The fruit also may not be developed enough for olive fruit fly to survive early in the summer; young, hard fruit are not preferred for oviposition (Burrack and Zalom 2008). Moreover, olive fruit fly populations are scarce in some interior valley regions with high summer temperatures (Wang, Johnson, Daane, Nadel 2009) (see page 29). These facts suggest that parasitoid survival might also be difficult in some regions where their host, the olive fruit fly larvae, is scarce during some seasonal periods. Wild versus domestic olives. The domestic olive is a distinct subspecies of wild olive, which has smaller fruit than most cultivated olives. As a result, fly maggots tunnel deeper inside the larger domestic olive. The ovipositors of specialized parasitoids (P. lounsburyi and P. ponerophaga) are too short to reach fly maggots feeding deep within the larger olives (Sime et al. 2007; Wang, Johnson, Daane, Yokoyama 2009; Wang, Nadel, Johnson, et al. 2009). The length of the ovipositor relative to the depth of the maggot within the fruit apparently limits the biocontrol agents ability to successfully parasitize certain hosts, a problem that has been well documented for other fruit fly parasitoids (Sivinski et al. 2001). Therefore, African parasitoids of olive fruit fly may fail to successfully establish on fruit flies in fleshier European cultivars, because their short ovipositors are adapted for foraging in small, wild, African olives. Surveys in wild and cultivated African olives provide support for this hypothesis. P. lounsburyi, U. africanus and B. celer are most commonly reared from wild olives (Copeland et al. 2004; Neuenschwander 1982), whereas
Ripe wild olives, left, collected in Africa, where olive fruit fly is considered to be native, are much smaller than the cultivated European varieties used throughout the world. Right, springbok and kudu graze among wild olive trees on a South Africa hillside. The African parasitoids that specialize on olive fruit fly found in small wild olives tend to have relatively short ovipositors that may not reach fly maggots deeper in the pulp of cultivated olives.
in cultivated olives, B. celer. with its much longer ovipositor, predominates, and the other species tend to be rare (Neuenschwander 1982). In the UC Berkeley quarantine studies, both D. longicaudata and D. kraussii reproduced well on cultivated olives, and these more generalist parasitoids have very long ovipositors (Sime, Daane, Messing, et al. 2006). Among the favorable characteristics of F. arisanus as a parasitoid of B. oleae are its relatively long ovipositor and the fact that it usually oviposits into eggs. Both features may help it circumvent the difficulties encountered by some larval parasitoids attacking B. oleae in larger olive cultivars. Natural enemy interactions. For best results natural enemies should coexist, but sometimes they interfere with each other. For example, the unexpected appearance of P. sp. nr. myopitae could potentially create a conflict with classical biological control efforts. Parasitoids that immobilize the host, including P. sp. nr. myopitae and B. celer, may have a competitive advantage over larval parasitoids that allow the host to continue to develop and grow after parasitoid oviposition, such as Psyttalia species. In quarantine experiments, researchers found that the egg-larval parasitoid F. arisanus prevailed in competition against two species of larval-pupal parasitoids, D. kraussii and P. concolor (Sime et al. 2008). The intrinsic competitive superiority of F. arisanus over larval-pupal parasitoids must be taken into consideration for its use in California. Insecticides and biological control. Insecticide use affects biological control programs (Mills and Daane 2005).
Repeated sprays of GF-120 Naturalyte NF Fruit Fly Bait (Dow AgroSciences, Indianapolis, Ind.) are used to control olive fruit fly. Although this spinosad bait is classified as a reduced-risk material, its frequent use may disrupt biological control. Nadel et al. (2007) investigated the impact of GF-120 on a green lacewing (Chrysoperla carnea [Stephens]), and showed that ingestion clearly poses some risk to lacewing populations due to adult mortality and reduced fecundity. Laboratory studies indicated that several important braconid parasitoids of fruit flies F. arisanus, Diachasmimorpha tryoni (Cameron) and Psyttalia fletcheri (Silvestri) would not feed on fresh GF-120 residues, but when the insecticide was directly applied there were high mortality rates (Wang et al. 2005).
Expectations in California
Biological control can be a practical, safe and economically effective means of fruit fly control, and its importance continues to grow in regions where pesticide use is less desirable (e.g., sustainable agriculture) or more restricted (e.g., urban trees). The research programs that we describe provide background information on natural enemy biology, and identify specific natural enemies for importation and evaluation, and for possible release into California. Over the coming years, researchers will better understand the level of controls expected from imported natural enemies, and will improve IPM programs to integrate biological controls with the insecticides currently used in olive management.
K.M. Daane is Cooperative Extension Specialist, Department of Environmental Science, Policy and Management, UC Berkeley; M.W. Johnson is Cooperative Extension Specialist and Entomologist, UC Riverside; C.H. Pickett is Research Entomologist, Biological Control Program, California Department of Food and Agriculture (CDFA); K.R. Sime is Assistant Professor, SUNY Oswego, N.Y.;
X.-G. Wang is Associate Specialist, Department of Environmental Science, Policy and Management, UC Berkeley; H. Nadel is Supervisory Entomologist, U.S. Department of Agriculture (USDA), Animal and Plant Health Inspection Service, Plant Protection and Quarantine program, Buzzards Bay, MA; J.W. Andrews Jr. was Quarantine Manager, College of Natural Resources, UC Berkeley; and K.A. Hoelmer is Research Entomologist and
Director, USDA Agricultural Research Service, European Biological Control Laboratory, Montpellier, France. We thank CDFA for funding this review; and the California Olive Committee, CDFA Biological Control Program (in collaboration with USDA) and USDA Cooperative State Research, Education, and Extension Services Pest Management Alternatives Program for funding olive fruit fly research.
References
Bokonon-Ganta AH, McQuate GT, Messing RH. 2007. Natural establishment of a parasitoid complex on Bactrocera latifrons (Diptera: Tephritidae) in Hawaii. Biol Control 42:36573. Burrack HJ, Zalom FG. 2008. Olive fruit fly (Diptera: Tephritidae) ovipositional preference and larval performance in several commercially important olive varieties in California. J Econ Entomol 101:7508. Calvitti M, Antonelli M, Moretti R, Bautista RC. 2002. Oviposition response and development of the eggpupal parasitoid Fopius arisanus on Bactrocera oleae, a tephritid fruit fly pest of olive in the Mediterranean basin. Entomol Exp Appl 102:6573. Canale A, Loni A. 2006. Host location and acceptance in P. concolor: Role of host instar. Bull Insectol 59:710. Collier T, Van Steenwyk R. 2003. Prospects for integrated control of olive fruit fly are promising in California. Cal Ag 57:2830. Copeland RS, White IN, Okumu M, et al. 2004. Insects associated with fruits of the Oleaceae (Asteridae, Lamiales) in Kenya, with special reference to the Tephritidae (Diptera). Bishop Mus Bull Entomol 12:13564. Daane KM, Johnson MW. 2010. Olive fruit fly: Managing an ancient pest in modern times. Annu Rev Entomol 55:15569. Daane KM, Sime KR, Wang, X-G, et al. 2008. Psyttalia lounsburyi (Hymenoptera: Braconidae), potential biological control agent for the olive fruit fly in California. Biol Control 44:7989. Foote RH, Blanc FL, Norrbom AL. 1993. Handbook of the Fruit Flies (Diptera: Tephritidae) of America North of Mexico. Cornell Univ Pr: Ithaca, NY. 571 p. Hancock DL. 1989. Pest status: Southern Africa. In: Robinson A, Hooper G (eds.). Fruit Flies: Their Biology, Natural Enemies and Control (Vol 3A). Amsterdam: Elsevier. p 518. Hoddle MS. 2004. Restoring balance: Using exotic species to control invasive exotic species. Conserv Biol 18:3849. Hoelmer KA, Kirk AA. 2005. Selecting arthropod biological control agents against arthropod pests: Can the science be improved to decrease the risk of releasing ineffective agents? Biol Control 34:25564. Johnson MW, Zalom FG, Van Steenwyk R, et al. 2006. Olive fruit fly management guidelines for 2006. UC Plant Prot Quart 16(3):17. Kapaun T, Nadel H, Headrick D, Vredevoe L. 2010. Biology and parasitism rates of Pteromalus nr. myopitae (Hymenoptera: Pteromalidae), a newly discovered parasitoid of olive fruit fly Bactrocera oleae. Biol Control 53:7685. Mills NJ, Daane KM. 2005. Biological and cultural controlsNonpesticide alternatives can suppress crop pests. Cal Ag 59(1):238. Moretti R, Calvitti M. 2003. Mortality by parasitization in the association between the egg-pupal parasitoid Fopius arisanus and Ceratitis capitata. Biocontrol 48:27591.
Nadel H, Daane KM, Hoelmer KA, et al. 2009. Nontarget host risk assessment of the idiobiont parasitoid Bracon celer (Hymenoptera: Braconidae) for biological control of olive fruit fly in California. Biocontrol Sci Technol 19:70115. Nadel H, Johnson MW, Gerik M, Daane KM. 2007. Ingestion of spinosad bait GF-120 and resulting impact on adult Chrysoperla carnea (Neuroptera: Chrysopidae). Biocontrol Sci Technol 17:9951008. Nardi F, Carapelli A, Dallai R, et al. 2005. Population structure and colonization history of the olive fruit fly, Bactrocera oleae (Diptera, Tephritidae). Mol Ecol 14:272938. Neuenschwander P. 1982. Searching for parasitoids of Dacus oleae (Gmel.) (Dipt., Tephritidae) in South Africa. J Appl Entomol 94:50922. Neuenschwander P, Bigler F, Delucchi V, Michelakis SE. 1983. Natural enemies of preimaginal stages of Dacus oleae Gmel. (Dipt., Tephritidae) in Western Crete. I. Bionomics and phenologies. Bollettino Laboratorio Entomologia Agraria Filippo Silvestri 40:332. Orsini MA, Daane KM, Sime KR, Nelson EH. 2007. Mortality of olive fruit fly pupae in California. Biocontrol Sci Technol 17:797807. Ramadan MM, Wong TTY, Beardsley JW. 1992. Reproductive behavior of Biosteres arisanus (Sonan) (Hymenoptera: Braconidae), an egg-larval parasitoid of the oriental fruit fly. Biol Control 2:2834. Rice R, Phillips P, Stewart-Leslie J, Sibbett G. 2003. Olive fruit fly populations measured in Central and Southern California. Cal Ag 57:1227. Rugman-Jones PF, Wharton R, van Noort T, Stouthamer R. 2009. Molecular differentiation of the Psyttalia concolor (Szpligeti) species complex (Hymenoptera: Braconidae) associated with olive fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae), in Africa. Biol Control 49:1726. Sime KR, Daane KM, Andrews JW, et al. 2006. The biology of Bracon celer as a parasitoid of the olive fruit fly. Biocontrol 51:55367. Sime KR, Daane KM, Kirk A, et al. 2007. Psyttalia ponerophaga (Hymenoptera: Braconidae) as a potential biological control agent for the olive fruit fly in California. Bull Entomol Res 97:23342. Sime KR, Daane KM, Messing RH, Johnson MW. 2006. Comparison of two laboratory cultures of Psyttalia concolor (Hymenoptera: Braconidae), as a parasitoid of the olive fruit fly. Biol Control 39:24855. Sime KR, Daane KM, Nadel H, et al. 2006. Diachasmimorpha longicaudata and D. kraussii (Hymenoptera: Braconidae), potential parasitoids of the olive fruit fly. Biocontrol Sci Technol 16:16979. Sime KR, Daane KM, Wang X-G, et al. 2008. Evaluation of Fopius arisanus as a biological control agent for the olive fruit fly in California. Agr Forest Entomol 10:42331. Sivinski J, Vulinec K, Aluja M. 2001. Ovipositor length in a guild of parasitoids (Hymenoptera: Braconidae) attacking Anastrepha spp. fruit flies (Diptera: Tephritidae) in Southern Mexico. Ann Entomol Soc Am 94:88695. Tzanakakis ME. 2006. Insects and Mites Feeding on Olive. Boston: Brill. 182 p.
Wang X-G, Bokonon-Ganta AH, Ramadan MM, Messing RH. 2004. Egg-larval opiine parasitoids (Hym., Braconidae) of tephritid fruit fly pests do not attack the flowerhead-feeder Trupanea dubautiae (Dip., Tephritidae). J Appl Entomol 128:71622. Wang X-G, Ekhlass J, McGraw BK, et al. 2005. Effects of spinosad-based fruit fly bait GF-120 on fruit fly and aphid parasitoids. Biol Control 35:15562. Wang X-G, Johnson MW, Daane KM, Nadel H. 2009. High summer temperatures affect the survival and reproduction of olive fruit fly (Diptera: Tephritidae). Env Entomol 38:1496504. Wang X-G, Johnson MW, Daane KM, Opp S. 2009. Combined effects of heat stress and food supply on flight performance of the olive fruit fly (Diptera: Tephritidae). Ann Entomol Soc Am 102:72734. Wang X-G, Johnson MW, Daane KM, Yokoyama VY. 2009. Larger olive fruit size reduces the efficiency of Psyttalia concolor, as a parasitoid of the olive fruit fly. Biol Control 49:4551. Wang X-G, Messing RH. 2003. Foraging behavior and patch time allocation by Fopius arisanus (Hymenoptera: Braconidae), an egg-larval parasitoid of tephritid fruit flies. J Insect Behav 16:593612. Wang X-G, Messing RH. 2004. Potential interactions among pupal and egg- or larval-pupal parasitoids of tephritid fruit fly. Env Entomol 33:131320. Wang X-G, Messing RH, Bautista RC. 2003. Competitive superiority of early acting species: A case study of opiine fruit fly parasitoids. Biocontrol Sci Technol 13:391402. Wang X-G, Nadel H, Johnson MW, et al. 2009. Crop domestication relaxes both top-down and bottomup effects on a specialist herbivore. Basic Appl Ecol 10:21627. Wharton RA. 1989. Classical biological control of fruitinfesting Tephritidae. In: Robinson A, Hooper G. (eds.). Fruit Flies: Their Biology, Natural Enemies and Control (Vol 3B). Amsterdam: Elsevier. p 30313. Wharton RA, Gilstrap FE. 1983. Key to and status of opiine braconid (Hymenoptera) parasitoids used in biological control of Ceratitis and Dacus spp. (Diptera: Tephritidae). Ann Entomol Soc Am 76:72142. Wharton RA, Trostle MK, Messing RH, et al. 2000. Parasitoids of medfly, Ceratitis capitata, and related tephritids in Kenyan coffee: A predominantly koinobiont assemblage. Bull Entomol Res 90:51726. Yokoyama VY, Cceres CE, Kuenen LPS, et al. 2010. Field performance and fitness of an olive fruit fly parasitoid, Psyttalia humilis (Hymenoptera: Braconidae), mass reared on irradiated Medfly. Biol Control 54:909. Yokoyama VY, Miller GT, Stewart-Leslie J, et al. 2006. Olive fruit fly (Diptera: Tephritidae) populations in relation to region, trap type, season and availability of fruit. J Econ Entomol 99:20729. Yokoyama VY, Rendn PA, Sivinski J. 2008. Psyttalia cf. concolor (Hymenoptera: Braconidae) for biological control of olive fruit fly (Diptera: Tephritidae) in California. Env Entomol 37:76473.
28
REVIEW ARTICLE
High temperature affects olive fruit fly populations in Californias Central Valley
Marshall W. Johnson
by Marshall W. Johnson, Xin-Geng Wang, Hannah Nadel, Susan B. Opp, Kris LynnPatterson, Judy Stewart-Leslie and Kent M. Daane
Olive fruit fly commonly infests olives in Californias Central Valley. Field studies indicate that trap counts for olive fruit fly adults in pesticidefree sites decrease in mid and late sum mer and then rebound from Septem ber to November. Part of this decline is associated with heat stress that the flies experience in midJuly and Au gust. Studies have shown that adult flies will die within a few days if they cannot access adequate amounts of water and carbohydrates. Flight ability is dramatically reduced when McPhail traps (Johnson et al. 2006). by pruning infested trees to facilitate The numbers of adults captured in the greater air movement in the summer, fly adults may use black scale hon Central Valley decline during the which results in significant desiccation eydew as a carbohydrate source to hottest periods of July and August and of first-instar crawlers (Daane and Calhelp them survive hot periods. Heat increase in September as temperatures tagirone 1989). decrease (Rice et al. 2003; Yokoyama However, the establishment of olalso affects the flys reproduction and et al. 2006) (fig. 1). For most insect speive fruit fly (Bactrocera oleae [Rossi]) immature stages within olive fruit. cies, a decline in trap counts suggests a (Diptera: Tephritidae) forced many Geographic information system (GIS) reduction in adult densities in an area. growers onto a weekly treatment remaps may be useful for predicting This is not initially the case with olive gime that runs from mid-June through fruit fly, whose behavior changes as harvest (September to December), the risk of olive fruit fly infestation. daily temperatures rise. using the spinosad product GF-120 Avidov (1954) reported that below NF Naturalyte Fruit Fly Bait (Dow he discovery in 1998 and subsequent AgroSciences) (Johnson et al. 2006). This 62F the adults are inactive. As temspread of the olive fruit fly through- management protoout the major olive-producing areas of col enables growers California dramatically affected the to deliver fruit with As temperatures surpass 84F, adult flies become pest management activities practiced by near-zero infestation increasingly agitated and egg laying is halted, growers. Prior to its introduction, the levels to the table olive major arthropod pests targeted for con- processors. Olives des- and above 95F they are motionless. trol in California olives were olive scale tined for oil pressing (Parlatoria oleae Colve) (Hempitera: Dimay have significant aspididae) and black scale (Saissetia oleae levels of infestation without an appreperatures increase above the threshold [Olivier]) (Hempitera: Coccidae) (Daane ciable decline in quality, as long as the temperature, adult activity increases. et al. 2005). Olive scale is well managed time between harvest and pressing is Normal activity, flight and egg laywith biological control due to the intro- minimal (Pereira et al. 2004; Torres-Villa ing occur between 73F and 84F. As duction and establishment of the paratemperatures surpass 84F, adult flies et al. 2003). sitoids Aphytis paramaculicornis DeBach become increasingly agitated and egg Adult behavior and survival and Rosen, and Coccophagoides utilis laying is halted, and above 95F they Olive fruit fly adults may be moniDoutt (Daane et al. 2005). Black scale is are motionless. Laboratory observatored with flat-panel sticky traps or mainly controlled in the Central Valley tions (M.W. Johnson, unpublished) also resources are unavailable. Olive fruit
An adult female olive fruit fly deposits an egg into olive fruit.
suggest that adults seek and remain near moisture sources as temperatures approach and surpass 95F. Reduced adult fly activity can result in lower trap counts in the field while maximum daily temperatures remain around 95F to 99F and the flies have access to adequate water and carbohydrate sources (Wang et al. 2009a). However, as the frequency at which daily maximum temperatures equal or surpass 100F increases, greater numbers of adults will die due to heat stress, especially when they cannot access adequate quantities of water and food (Wang et al. 2009a, b) (fig. 2). Although adult females may ingest liquid from punctures they make in olive fruit, this secretion does not provide the needed carbohydrates to help them survive heat-induced stress (Johnson and Nadel, unpublished data).
One might assume that acquisition of adequate amounts of food and water would be easy for olive fruit fly adults, which are strong flyers. Using a customdesigned flight mill, Wang et al. (2009b) reported that adults of both sexes held for 7 days at 75F (constant temperature) and provided with ample food (honey and hydrolyzed yeast) and water, were able to fly uninterrupted for an average of 2,164.8 228.8 yards during a mean period of 1.54 0.16 hours (fig. 3). Nonetheless, heat stress and lack of water and food can affect flight ability. Olive fruit fly adults that were subject to the same conditions as described for 7 days and then to water only or no food and water in diurnal temperature regimes (65F at night; 95F or 100F during the day) for 24 hours before the flight test did not perform as well as the control group (fig. 3). All stressed
groups of tested flies flew significantly shorter distances ( 42%) than the control (F6,252 = 62.7, P < 0.01). Additionally, individual flies that were denied food and water from the time that they emerged as adults and were held at either 65F at night and 95F, or 100F, during the day for 1 to 2 days, flew significantly shorter distances ( 92%) than the flies provided no food and water for 24 hours after having access to food and water for 7 days (fig. 3). In a worst-case scenario, an adult fly that emerges in mid-August in the Central Valley may commonly experience maximum daily temperatures over 100F for 3 consecutive days (LynnPatterson 2006). Without food or water immediately available, an adult will only be able to fly an average of 16.4 4.4 yards to locate these resources in a dry and unexplored landscape.
Sites
2,500
Treated Untreated
Mean total ies/trap/week
2,000
(A) 75F, food and water (B) 95F, water, 24 hours (C) 100F, water, 24 hours (D) 95F, no resources, 24 hours (E) 100F, no resources, 24 hours (F) 95F, no resources (G) 100F, no resources b b
0
10 17 24 1 8 15 22 29 5 13 20 27 4 11 18 25 1 8 15 22 29 6 13 20 27 3 10 17 24 31 7 14
Mean distance (yards)
1,500
1,000 bc c 500
April
May
June
July
Aug
Sept
Oct
Nov
Fig. 1. Average olive fruit fly populations at nine untreated sites (e.g., urban, landscape and abandoned commercial plantings) and five treated (with GF-120) commercial sites in Fresno and Tulare counties during the 2003 growing season (Johnson, Nadel and Stewart-Leslie, unpublished data). Fig. 2. Mortality of olive fruit fly adults subjected to 1 to 3 days exposure to 95F and 100F, in the absence of food and with and without access to water (Wang et al. 2009b). Different letters above columns representing the same temperature/resource treatment indicate significant differences (P < 0.05; Tukeys HSD test) within the exposure duration.
d 0
90 80 70 95F, water 100F, water 95F, no resources 100F, no resources b b c
Treatment
Adult mortality (%)
60 50 40 30 20 a 10 a 0 1 2 a a b a
Days of exposure
Fig. 3. Mean distances flown by olive fruit fly adults exposed to various temperatures and resources. Flies (A-E) were preconditioned for 7 days at 75F with ample food and water prior to treatment. Treatments were: (A) no treatment (control); (B) preconditioned at 95F, then 24 hours of water only; (C) preconditioned at 100F, then 24 hours of water only; (D) preconditioned at 95F, then 24 hours with no resources; (E) preconditioned at 100F, then 24 hours with no resources; (F) no preconditioning, held from 1 to 2 days at 95F with no resources; and (G) no preconditioning, held from 1 to 2 days at 100F with no resources (Wang et al. 2009b). Different letters above columns indicate significant differences (P < 0.05; Tukeys HSD test).
30
(W) (W) (H) (H)
Experimental setup shows (A) the typical distribution of five olive fruit fly adults (circled) within an observation chamber, with cotton wicks and water (W) and honey (H) at a cool temperature (80F) and 20% relative humidity, and (B) the congregation of olive fruit fly adults (circled) around a water wick (W) when the temperature is hot (99.5F) and 37% relative humidity.
Mean distance own uninterrupted (yards)
2,000 a
a 95F, water 100F, water 95F, no resources 100F, no resources ab
1,500
1,200
900 a 600 a
b b ab ab b b b
300
0 1 2 3
Days of exposure
Fig. 4. Mean distances flown by olive fruit fly adults subjected to 1 to 3 days exposure to 95F and 100F, in the absence of food and with and without access to water (Wang et al. 2009b). Different letters above columns representing the same temperature/resource treatment indicate significant differences (P < 0.05; Tukeys HSD test) within the exposure duration.
Such a fly would have an 84% chance of dying in the first 24 hours, and of those that did survive only about 25% would be able to fly (Wang et al. 2009b). Additionally, when olive fruit fly adults were held at 65F at night and 95F or 100F during the day over a 3-day period with either water alone or no food or water, those flies that survived one day could fly significantly farther than those that survived 3 days (F2,407 = 18.7, P < 0.01) (fig. 4).
Egg and larval survival
Fly flight is measured using (A) a custom-designed flight mill setup with computer; (B) an individual flight mill unit; (C) a beam that rotates during insect flight; and (D) a tethered fly fastened to a rotating beam.
Reproductive dormancy in olive fruit fly subsides as greater numbers of mature fruit appear within the orchard,
commonly in late July and early August in California (Burrack and Zalom 2008; Wang et al. 2009a). During periods of high maximum daily temperatures (3 consecutive days at 100F or above in July and August) (Lynn-Patterson 2006), mated adult females may lay their eggs in developing olives prior to morning temperatures reaching 95F. No eggs are deposited during the night, even when temperatures are cool enough for normal activity (Avidov 1954; Wang et al.
2009a). Eggs are deposited just beneath the fruit epidermis and may be exposed to high temperatures, depending on where an individual fruit is located on the tree (Wang et al. 2009a). Laboratory studies showed that adult females held under different diurnal temperature regimes (65F at night and 75F, 95F or 100F during the day) laid similar numbers of eggs when the temperature was 65F and the experimental chamber was illuminated (F2,55 = 0.2,
P = 0.852). However, under illumination and higher temperatures, females laid significantly fewer eggs at 95F (about four per female) than at 75F (about 12 per female) (F1,38 = 8.4, P = 0.006), and no eggs were laid at 100F (Wang et al. 2009a). Even after eggs are deposited within olive fruit, they are still susceptible to the high temperatures common in Central Valley orchards. Eggs within fruit held at 65F (night) and 75F (day) developed into first-instar larvae after 6 days (Wang et al. 2009a). In contrast, eggs within fruit subjected to 65F (night) and 95F (day) had a 49% mortality rate, and of the first-instar larvae that did develop, none became second instars. When subjected to 65F (night) and 100F (day), no eggs hatched after 10 days exposure and all died. The overall finding was that egg (F3,57 = 2472, P < 0.001) and first-instar (F3,57 = 2472, P < 0.001) mortality increased as exposure time increased (Wang et al. 2009a). Later field studies showed that maximum daily temperatures in olive trees in the Central Valley (Parlier) varied depending on whether measurements were taken within the canopy interior or the east or west perimeter. Mean temperatures recorded on the west side of the tree canopy in August 2007 were 108F (and over 104F for 26 days) compared to 101F (and over 104F for 13 days) on the east side, and 96F (and never over 104F) within the canopy interior (F2,90 = 52.7, P < 0.001). All of these temperatures are high enough to impose some level of mortality on olive fruit fly eggs and larvae. Field studies
in the same locality in mid- and late summer 2007 and 2008 showed that less than 2% of offspring from eggs laid in olives completed development to the adult stage (Wang et al. 2009a).
Scale honeydew and heat stress
100
Olive fruit y survival (%)
80 60 40 20 0
Honeydew only Honeydew and water Honey only Honey and water No food
This information suggests that it is difficult for olive fruit fly adults to survive the high summer temperatures in the Central Valley. Water may commonly be found within or near most orchards from a variety of sources, such as morning dew, creeks, ponds, irrigation water (ditches and canals), sprinklers, drip tape and fan jets. However, fly adults also need carbohydrates to survive heat stress. Honeydew (fresh or dry) produced by black scale is a common carbohydrate source in olive orchards. Our laboratory tests have shown that fly adults provided with honey and water, or black scale honeydew and water, survive temperatures of 65F (night) and 97.5F (day) with minimal mortality compared to adults only provided honey alone, honeydew alone, or no food and water over 5 days (F4, 36 = 189.9, P < 0.0001) (fig. 5) (M.W. Johnson and H. Nadel, unpublished data). The carbohydrate source alone did not reduce the impact of heat on survival. Flies that had food resources (honeydew or pure honey) but no water suffered mortality similar to those flies without food or water. There was a significant interaction between carbohydrate source and days of exposure (F20, 180 = 33.3, P < 0.0001). These results are similar to what we have observed in our laboratory and field studies on olive fruit fly when 50% honey water was used as a carbohydrate source. These findings are significant because they suggest that olive fruit fly adults could use black scale honeydew to help them survive periods of high temperature in the Central Valley. The management of black scale populations via cultural controls such as the pruning of interior canopies may also contribute to the management of olive fruit fly adults.
Temperature maps and fly activity
Geographic information systems (GIS) enable the examination of temperFig. 5. Survival of olive fruit fly adults when ature trends over specific areas based held at 65F (night) and 97.5F (day) with access to various combinations of water, honey on defined criteria, such as temperature and black scale honeydew, or no food or water. levels for specific time intervals. The
Days of exposure
examination of temperature trends in olive-producing areas in the Central Valley over 10 years (19922001) revealed that it was quite common for temperatures to be greater than 100F for 3 consecutive days during mid-July and August (fig. 6) (Lynn-Patterson 2006). On the California coast, these trends were rarely observed. Over this time period, temperatures greater than 100F for 3 consecutive days were more common in the southern (San Joaquin Valley) than the northern (Sacramento Valley) Central Valley (see http:/ /arcims.gis.uckac.edu/CIMIS). By September, most of the Central Valley rarely had 3 consecutive days greater than 100F (fig. 6).; in 2003, olive fruit fly surpassed one adult per trap per week at the end of August and continued to increase into November (fig. 1). Growers and consultants may wish to use these maps to determine if they can temporarily halt insecticide treatments for olive fruit fly adults during July and August. However, there are many factors other than temperature that influence whether olive fruit fly will be a problem in a particular olive orchard. Olive fruit fly adults with access to adequate sources of water and carbohydrates can survive heat stress in large numbers and will be able to fly long distances (more than 1,000 yards) even when stressed. Growers who consider halting their control programs, especially in the San Joaquin Valley, should take under consideration the irrigation schedules and infestation levels of black scale and other insects that might produce honeydew within their own and neighboring orchards. Also important is the proximity of irrigation canals, creeks, ponds and rivers, as well as abandoned orchards or untreated olives trees used for landscaping, which can serve as an infestation source of olive fruit fly. Morning dew in the orchard may provide a moisture source for flies, and weedy undergrowth in the orchard or neighboring crops can afford some relief from the heat. Perhaps the most useful information that one can obtain from the GIS maps is knowing when temperatures historically have dropped to low levels that would be conducive to olive fruit fly activity and survival in a particular area. As temperatures decline at the end
32
July 15
Aug. 15
Sept. 15 Occurrences
0 12 35 68 910
Fig. 6. Mean temperature patterns in California over 10 years (19922001), showing number of years (occurrences) with maximum temperatures greater than or equal to 100F for 3 consecutive days ending on July 15, Aug. 15 and Sept. 15 (Lynn-Patterson 2006).
of August, olive fruit are increasing in size and maturing (Martin and Sibbett 2005). Olive fruit fly adults prefer to lay their eggs in the largest olives available (Neuenschwander et al. 1985). As flies return to normal activity in late summer, the olives remaining on the trees are at greater risk of infestation than at anytime during the summer, and protecting the fruit then is of prime consideration.
Future directions
Research on the ecology and management of olive fruit fly is continuing. A better understanding of the abilities of olive fruit fly adults to disperse among orchards in the summer would
be helpful. Given that olive fruit fly adults need carbohydrate sources to survive heat stress, it may be best to continue treating with GF-120 in July and August. The adults are attracted to the sweet fruit fly bait in the GF-120. If stressed flies seek a carbohydrate source in summer, it may be assumed that they would then seek out available bait residues in GF-120. If this is true, the GF-120 may be having a greater impact than realized. This needs to be determined. Also of importance is the impact of summer heat either directly or indirectly on parasitoid natural enemies that are now being released as part of a classical biological control program for olive fruit fly control (see page 21).
M.W. Johnson is Cooperative Extension Specialist and Entomologist, Department of Entomology, UC Riverside; X.-G. Wang is Associate Specialist, Department of Environmental Science, Policy and Management, UC Berkeley; H. Nadel is Supervisory Entomologist, U.S. Department of Agriculture Animal and Plant Health Inspection Service, Plant Protection and Quarantine program, Buzzards Bay, MA; S.B. Opp is Associate Vice President, Academic Programs and Graduate Studies, California State University, East Bay; K. LynnPatterson is GIS Academic Coordinator, UC Kearney Agricultural Center, Parlier; J. Stewart-Leslie is Manager, Consolidated Central Valley Table Grape Pest and Disease Control District, Exeter, CA; and K.M. Daane is Cooperative Extension Specialist, Department of Environmental Science, Policy and Management, UC Berkeley.
References
Avidov Z. 1954. Further investigations on the ecology of the olive fly (Dacus oleae, Gmel.) in Israel. Ktavim 4:3950. Burrack HJ, Zalom FG. 2008. Olive fruit fly, Bactrocera oleae (Gmel.), ovipositional preference and larval performance in several commercially important olive varieties in California. J Econ Entomol 101:7508. Daane KM, Caltagirone LE. 1989. Biological control of black scale in olives. Cal Ag 43(1):911. Daane KM, Rice RE, Zalom FG, et al. 2005. Arthropod pests of olive. In: Sibbett GS, Ferguson L. Olive Production Manual (2nd ed.). UC ANR Pub 3353. p 10514. Johnson MW, Zalom FG, Van Steenwyk R, et al. 2006. Olive fruit fly management guidelines for 2006. UC Plant Protect Quart 16:17.
Lynn-Patterson K. 2006. Interactive climate maps for olive fly management decisions. http://arcims.gis. uckac.edu/CIMIS. Martin GC, Sibbett GS. 2005. Botany of the olive. In: Sibbett GS, Ferguson L. Olive Production Manual (2nd ed.). UC ANR Pub 3353. p 157. Neuenschwander P, Michelakis S, Holloway P, Berchtold W. 1985. Factors affecting the susceptibility of fruits of different olive varieties to attack by Dacus oleae (Gmel.) (Dipt., Tephritidae). J Appl Entomol 100:17488. Pereira JA, Alves MR, Casal S, Oliveira MBPP. 2004. Effect of olive fruit fly infestation on the quality of olive oil from cultivars Cobrancosa, Madural and Verdeal Transmontana. Ital J Food Sci 16:35565. Rice R, Phillips P, Stewart-Leslie J, Sibbett S. 2003. Olive fruit fly populations measured in Central and Southern California. Cal Ag 57(4):1227.
Torres-Villa LM, Rodriguez-Molina MC, Martinez JA. 2003. Olive fruit fly damage and olive storage effects on paste microflora and virgin olive oil acidity. Grasas Aceites 54:28594. Wang X-G, Johnson MW, Daane KM, Nadel H. 2009a. High summer temperatures affect the survival and reproduction of olive fruit fly (Diptera: Tephritidae). Env Entomol 38:1496504. Wang X-G, Johnson MW, Daane KM, Opp S. 2009b. Combined effects of heat stress and food supply on flight performance of olive fruit fly (Diptera: Tephritidae). Ann Entomol Soc Am 102:72734. Yokoyama VY, Rendon P, Sivinski J. 2006. Psyttalia cf. concolor (Hymenoptera: Braconidae) for biological control of olive fruit fly (Diptera: Tephritidae) in California. Env Entomol 37:76473.
RESEARCH ARTICLE
Mediterranean clonal selections evaluated for modern hedgerow olive oil production in Spain
Paul M. Vossen
by Joan Tous, Agusti Romero, Juan Francisco Hermoso and Antonia Ninot
Traditional olive oil production is limited by its high cost, mainly due to labor expenses for harvesting and pruning. A new olive planting system based on hedgerows and harvesting machines could decrease production costs while maintaining high quality. To improve the efficiency of the continuousstraddle mechanical harvesters, vigor must be managed to limit tree size. However, few cultivars are adapted to this system. Selections from three cultivars are typically used in these superhigh density orchards. We fieldtested Arbequina i18, Arbosana i43 and Koroneiki i38 in an irrigated, superhighdensity planting system in Catalonia (northeast Spain). We present a review of 6 years of horticultural data and summarize sensory characteristics and other properties of the resulting olive oils.
Olive trees have been cultivated for centuries in Mediterranean climates, including Californias Central Valley (shown). New super-high-density hedgerow systems allow for mechanical harvesting, greatly reducing labor costs.
he olive tree, olive fruit and olive oil have been at the core of Mediterranean agriculture and trade since early cultivation times, providing sustenance to various cultures and civilizations of the Mediterranean Basin. Over the last few decades, olive (Olea europaea) cultivation has undergone important technological changes, which have involved a reduction in the number of olive oil varieties used, and an increase in the density of new plantations that is linked to improvements in harvesting machinery and irrigation systems. In the early 1990s, a new design and management strategy for olive orchards, the super-high-density hedgerow system, appeared in Catalonia (northeast Spain). Later it was introduced into other Spanish regions and
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other countries. Clonal selections of local varieties were planted in new olive orchards with tree densities ranging from 600 to 1,000 trees per acre (1,500 to 2,500 per hectare) to test the suitability of the plants to mechanization and the production of high-quality, extra-virgin olive oil. Traditional olive orchards have 80 to 200 trees per acre (200 to 500 per hectare). Just a few olive varieties have been compared for their adaptability to high-density plantings and continuous mechanical harvest. Our program at the Institut de Recerca i Tecnologia Agroalimentaria (IRTA) screened three old Mediterranean olive
varieties Arbequina and Arbosana from Catalonia and Koroneiki from Crete (Greece) to identify those with outstanding characteristics such as compact growth habits, low-medium vigor, early maturity and excellent oil quality (Tous et al. 2003). Agronomical evaluations in Spain and other countries have shown that these IRTA clones are precocious (bearing their first crop at an earlier age than standard cultivars), achieve higher yields earlier after planting and produce extra-virgin oil of excellent quality.
California olive orchards
Editors note: More than 12,000 acres of olives have been planted in California using the super-high-density system. Research in California is inconclusive about the long-term viability of super-high-density olive culture under California growing conditions; further field studies based in the state can address these questions.
Olives were introduced in California by the Catalan Franciscan fathers, who planted olive trees in gardens adjacent to their missions. Their olives and oil were appreciated not only as food but also as an element in liturgical celebrations. Today, the predominant table olive industry in California is supported by classic cultivars introduced for their suitability to traditional and intensive table olive orchard systems (Tous and Ferguson 1997; Vossen 2007). In California, the industry generally plants
five cultivars (Mission, Manzanillo, Sevillano, Ascolano and Barouni) to produce black-ripe olives (Connell 2005). Mission trees were likely introduced to California during Franciscan times, via Mexico in 1769 (Sutter 2005). Olive planting for oil production, by contrast, has grown from negligible acreage in 1996 to approximately 16,000 acres (6,400 hectares) by 2008. Most of this acreage, 12,000 acres (4,800 hectares), is planted in super-high-density orchards with 560 to 870 trees per acre (1,400 to 2,175 per hectare) (UC Davis Olive Center 2009). Most high-density California olive plantings are three releases of IRTAs clonal plant material from the Mas de Bover research station in Catalonia, Spain, the initial selections from their olive improvement program started in the mid-1980s. The IRTA clonal varieties currently available are Arbequina i-18, Arbosana i-43 and Koroneiki i-38, propagated in California by a few authorized nurseries. The success of these early clonal selections and the superhigh-density system is also evidenced by their early adoption in traditional olive oilproducing countries, such as Spain, Portugal, Tunisia and Morocco, as well as diverse, nontraditional olivegrowing regions that are beginning to produce extra-virgin olive oils of
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TABLE 1. Horticultural characteristics of three olive tree clones tested in a super-high-density planting system in Catalonia, Spain Characteristics Vigor Growth habit Canopy density Precocity of bearing Productivity Fructification Harvest season Arbequina i-18 Low Semi-erect Compact Early Very high and regular In clusters Early, midseason* Arbosana i-43 Very low Open Compact Early Very high and regular In clusters Late Koroneiki i-38 Medium Open Compact Early High In clusters Midseason
* Maturation occurs in Catalonia from about mid-November to mid-December. Matures about 3 weeks later than Arbequina.
remarkable quality such as California, Chile and Australia. We describe the performance and limitations of these olive oil clones in comparative field trials performed in an irrigated, super-high-density system in Catalonia, which supports their adoption in modern orchards. We also contribute additional information to help define the suitable orchard design and management of super-high-density plantings in California.
Horticultural characteristics
The clone Arquebina i-18 was obtained in 1997 in a program to identify and select outstanding individuals of Arbequina, the most important cultivar in Catalonia (160,000 acres [65,000
B
hectares]) from traditional orchards located in the PDOs (protected designations of origin) of Les Garrigues and Siurana in northeast Spain. Arbosana i-43 was selected in 1987 from surveys of the Arbosana cultivar in the Alt Peneds region in Catalonia. The clone Koroneiki i-38 was selected in 1990 from trees of this Greek variety at the Mas de Bover research station. Morphological descriptions of the tree, leaf, fruit and endocarp for these cultivar clones have been published (Tous et al. 1999; Tous and Romero 2000, 2002).
Crop performance
The first comparative field trial with these clones in super-high-density hedgerow orchards was planted in
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The growth habit of 11-year-old trees is shown for the IRTA clones (A) Arbequina i-18 (B) Arbosana i-43 and (C) Koroneiki i-38, in a hedgerow, super-high-density planting system in 2009, in Spain.
As the newly planted super-high-density orchards in California enter their optimal olive oil production phase, it will be interesting to compare and follow experiences and observations with other regions.
Tarragona in 1998 (Tous et al. 2003, 2008) (table 1). Yields. Differences between varietals in cumulative fruit yield became evident during early years of the trial (table 2). In Tarragona, the highest cumulative yields were measured for Arbequina i-18 (31,875 pounds per acre) followed by Arbosana i-43 (26,470 pounds per acre) and Koroneiki i-38 (22,361 pounds per acre). In a similar trial in Cordoba (Andalusia, southern Spain), Arbequina i-18, Arbosana i-43 and Koroneiki i-38 showed higher mean harvest yields (3 to 6 years after planting) than other varieties tested (data not shown) (Len et al. 2006); in this southern location Koroneiki i-38 was the most precocious (table 2). During the first years of both trials, the influence of environment on precocity and average crops achieved was larger in Cordoba due to the higher vegetative tree growth in this province. The mean harvest of super-highdensity cultivars in Tarragona was 4,397 pounds per acre (3rd year), 4,205 pounds per acre (4th year; frost on trees affected productivity), 10,344 pounds per acre (5th year) and 7,291 pounds per acre (6th year), all similar to harvests obtained in other high-density orchards in Spain. The high yields observed in early years of the Spanish trials and commercial orchards are not sustainable. Under the favorable growing conditions that foster vigorous tree growth, a reduction in potential production occurs in the 6th to 8th years, with averages of 7,138 to 8,030 pounds per acre,
TABLE 2. Annual and cumulative yields of IRTA olive clones planted in 1998 (Tarragona, Catalonia) and 2000 (Cordoba, Andalusia), Spain, in a super-high-density planting system 2 and 6 years after planting, respectively Arbequina i-18 Year Second Third Fourth Fifth Sixth Average (3th6th) Cumulative yield (lb/acre) Arbosana i-43 Koroneiki i-38
Tarragona Cordoba Tarragona Cordoba Tarragona Cordoba . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . lb/acre* . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1,102 6,002 4,428 12,038 8,305 7,693 31,875 0 13,203 12,527 17,957 5,519 12,302 49,207 803 4,771 2,833 12,173 5,890 6,537 26,470 273 15,305 7,990 17,279 6,583 11,790 47,431 0 2,416 5,356 6,822 7,678 5,568 22,361 3,213 18,502 5,440 11,170 4,027 9,786 42,354
* 1 lb/acre = 1.1209 kg/ha. In the 4th year (2002), crop yield was slightly lower due to frost problems in Tarragona (December 2001). Source: Tous et al. 2003, 2008; Len et al 2006.
TABLE 3. Vegetative and productive characteristics of three olive cultivars growing in a 5-year-old, super-high-density orchard in Catalonia, Spain, 20002003 (2nd5th year after planting) Cumulative Canopy volume yield (5th year) (2nd-5th year) Yield efficiency ft3/acre 192.389ab 168.795b 189.674ab lb/acre 23.539a 21.330ab 14.594c lb/ft3 0.12a 0.12a 0.07bc
Cultivar Arbequina i-18 Arbosana i-43 Koroneiki i-38
Suckers (4th year) 0.4c 1.4b 5.2a
TCSA* (5th year) in2 5.54c 5.85bc 7.67a
* Trunk cross-sectional area. 1 inch2 = 6.4516 cm2; 1 ft3/acre = 0.0700 m3/ha; 1 lb/acre = 1.1209 kg/ha; 1 lb/ft3 = 16.0185 kg/m3. Sum of first yields (2nd to 5th year) per cubic foot of canopy volume at 5th year (2003). Mean separation within columns by Duncans multiple range test, P < 0.05.
usually due to shade and limited ventilation in the tree canopies (Tous et al. 2010). The yields of 7- to 10-year-old orchards are more variable and depend on management of the canopy volume, which should not exceed 143,000 to 171,500 cubic feet per acre to facilitate movement of the over-the-row harvesters. Vigor. We observed the lowest tree vigor (trunk cross-section, canopy volume and sucker emission) in Arbosana i-43 and Arbequina i-18 (table 3). Koroneiki i-38 is notorious for being more vigorous and producing more suckers than the other cultivars. The yield efficiency of each varietal clone was measured to determine the balance between productive and vegetative activity during the early bearing phase. The highest index scores were observed in Arbequina i-18 and Arbosana i-43 (0.12 pound per cubic foot), followed by Koroneiki i-38 (0.07 pound per cubic foot). Koroneiki i-38 showed a higher tendency to vegetative growth, and the crop was irregular among trees during the first years of the trial. Mechanical harvest. Several intrinsic varietal characteristics, such as growth habit and canopy width, influence the efficiency of fruit removal during mechanical harvest. Our selections display two growth habit categories: semi-erect (Arbequina i-18) and open canopy (Arbosana i-43 and Koroneiki i-38). Straddle machines or grape harvesters perform better than trunk shakers for these cultivars. More than 90% of the fruit was removed in all cultivars, independent of their size, position in the canopy and maturation index. By contrast, the efficiency of trunk-shaking harvesters is clearly influenced by growth habit (Pastor et al. 1998), and yield is improved with an erect or semierect tree shape, large fruits and low fruit removal force. Disease. Arbequina i-18 is more sensitive than the other selections to olive leaf spot (Spilocaea oleagina) when planted in coastal environments and humid valleys. Arbequina i-18 is more tolerant than the other two cultivars to frost, while Koroneiki i-38 is the most sensitive.
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Harvest time. Gradual fruit ripening and maturation is commonly observed in the three cultivars, although this parameter is highly influenced by tree fruit load and seasonal conditions as well as geographical location. Optimal harvest time is different for each of the cultivars: Arbequina i-18 is optimal in Catalonia from mid-November to midDecember, Koroneiki i-38 matures in late December and Arbosana i-43 in mid-January. Fruit and oil characteristics. Arbequina i-18 produced larger fruits than the other two cultivars (table 4). The pulp/stone ratio was higher for Arbosana i-43 and Arbequina i-18, followed by Koroneiki i-38. Fruit water content ranged between 56.0% in Koroneiki i-38 and 61.1% in Arbosana i-43. Oil content expressed as percentage of dry weight was higher in Arbequina i-18 (54.4%), followed by Koroneiki i-38 (52.4%) and Arbosana i-43 (50.7%). The three clonal selections produced extra-virgin olive oil of excellent quality. The fatty acid composition of Arbequina i-18 and Arbosana i-43 oils was similar (table 5). Koroneiki i-38 oil is characterized by a higher content of oleic acid (more than 76%) at the expense of palmitic and linoleic acid, which contribute to longer shelf life. Arbosana i-43 and Koroneiki i-38 oils were consistently richer in polyphenols than Arbequina i-18. When compared at the organoleptic sensory level (fig. 1), Arbequina i-18 oil was the most balanced of the three, with a medium fruity intensity, balanced in the palate and an outstanding sweetness. Koroneiki i-38 produced the most fruity, green, bitter and pungent oil of
A
Apple Fruity Green almond
TABLE 4. Fruit characteristics of three IRTA clones tested in an irrigated, super-high-density planting system in Catalonia, Spain, from trees 3 to 7 years old, 20012005 Pulp/stone ratio 4.31 0.59 4.69 0.54 3.44 0.84
Cultivar Arbequina i-18 Arbosana i-43 Koroneiki i-38
Fruit weight g 1.72 0.18* 1.59 0.37 0.90 0.14
Oil content % fresh weight 21.9 1.0 19.8 0.8 22.9 0.8
Moisture % 60.1 3.0 61.1 2.2 56.0 2.3
Oil content % dry weight 54.4 2.5 50.7 2.8 52.4 3.4
* Mean values standard error (SE).
TABLE 5. Olive oil characteristics* of three IRTA clones tested in an irrigated, super-high-density planting system in Catalonia, Spain, from trees 5 to 6 years old, 2003 and 2004 Palmitic Oleic acid, Linoleic Linolenic Total acid, C16:0 C18:1 acid, C18:2 acid, C18:3 polyphenols ...................%................... Arbequina i-18 Arbosana i-43 Koroneiki i-38 14.5a 13.6a 11.4b 69.4c 73.0b 76.6a 11.1a 7.9b 6.89c 0.72b 0.9a 0.93a ppm cafeic acid 234b 343a 400a
Cultivar
Bitterness K225 0.2a 0.30a 0.45b
Oil stability hours 9.10b 12.8ab 15.23a
* Oil characteristics: main fatty acid composition (%), total polyphenols (ppm cafeic acid), bitterness (K225) and oil stability. Oil stability against oxidation, applying Rancimat method (hours at 120C). Mean separation within columns by Duncans multiple range test, P < 0.05.
the three, and Arbosana i-43 oils had an intermediate palate profile. Oil composition and flavor change as the olive fruit develops. The distinctive and contrasting sensory attributes of the extravirgin oils from each varietal allows for unique blends with a wide range of interesting sensory characteristics.
Field observations
Initial observations from the Mas de Bover cultivar trials and orchard design evaluations, initiated in the 1980s, have been validated by the worldwide adoption of IRTAs clonal selections. The three initial selections described here have been planted in new high-density (121 to 242 trees per acre) and superhigh-density (over 600 trees per acre) olive tree orchards around the world, and most recently California.
B
Apple Fruity Twiggy
The most consistent plant characteristics and performance, as observed in super-high-density orchards around the world, can be summarized as follows: Arbequina i-18. This highly productive variety is early bearing with little alternating bearing. It is considered frost resistant and adaptable to different climatic and soil conditions, and is adaptable to high-density and superhigh-density hedgerow orchards. Its semi-erect growth habit facilitates its training on a central leader. It produces medium-fruited extra-virgin oil that is balanced in the mouth; the sweet attribute is outstanding and easily appreciated by new consumers. Its commercialization can be monovarietal or blended with other oils. Arbosana i-43. This is an earlybearing cultivar with high productivity.
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Apple Fruity Artichoke
Ripe fruits
Green grass
Ripe fruits
Green leaves
Ripe fruits
Green leaves
Sweetness
Bitterness
Sweetness
Bitterness
Sweetness
Bitterness
Astringency
Pungency
Astringency
Pungency
Astringency
Pungency
Fig. 1. Sensorial profiles of olive oils from three IRTA clones: (A) Arbequina i-18, (B) Arbosana i-43 and (C) Koroneiki i-38. The green polygon represents the intensity of each taste attribute scored on a 10-point scale.
Arbequina i-18
Arbosana i-43
Fruit of three clones used in super-highdensity planting systems. Arbequina i-18 and Arbosana i-43 are native to Catalonia, Spain, and Koroneiki i-38 is native to Greece.
Koroneiki i-38
sources of novel germplasm to produce olives of improved agronomic performance and desirable olive oil sensory attributes. As the newly planted super-highdensity orchards in California enter their optimal olive oil production phase, it will be interesting to compare experiences and observations with other regions in terms of economic viability, orchard management and sustainability, natural resource utilization and extra-virgin oil qualities.
Due to its low vigor, it adapts well to hedgerow systems for olive growing. Sensitive to frost, its fruit is small and ripens several weeks later than Arbequina. It produces intense, greenfruited virgin oil with high levels of bitterness, spiciness and astringency. Due to its higher polyphenol content, it is particularly interesting for blending and to stabilize and prolong the shelf life (time to rancidity) of the milder Arbequina oil. Koroneiki i-38. This is a productive and early-bearing cultivar. It is considered drought resistant but frost sensitive, and well suited to hot growing areas. It is tolerant to olive leaf spot and has very small fruit, which ripen after Arbequina but before Arbosana. It produces quite-stable extra-virgin oils, rich in oleic acid and polyphenols, with intense green color and bitterness, and a long shelf-life.
Olive tree breeding program
for varietal characteristics that can improve productivity, a low vigor/compact growth habit, disease resistance and extra-virgin olive oil with high levels of antioxidants. IRTA recently initiated a project to catalogue a collection of ancient trees (estimated 500 to 700 years old) in local orchards around northeast Spain that contain individual trees of unclear varietal origin, as potential
J. Tous is Agricultural Engineer, A. Romero is Agricultural Engineer, J. Francisco Hermoso is Agricultural Engineer, and A. Ninot is Agricultural Engineer, Institut de Recerca i Tecnologia Agroalimentaria (IRTA) Mas de Bover research station, Constant, Catalonia, Spain. We are grateful to the owners of the La Boella farm (La Canonja, Spain) for their collaboration in this trial.
References
Connell JH. 2005. History and scope of the olive industry. In: Sibbett GS, Ferguson L (eds.). Olive Production Manual (2nd ed.). UC ANR Pub 3353. Oakland CA. p 110. Len L, de la Rosa R, Guerrero N, et al. 2006. Ensayos de variedades de olivo en plantacin de alta densidad. Fruticultura Profesional 160:216. Pastor M, Humanes J, Vega V, Castro A. 1998. Diseo y manejo de plantaciones de olivar. Monografas, 22/98. Ed. Consejeria de Agricultura y Pesca. Junta de Andaluca, Sevilla. Sutter EG. 2005. Olive cultivars and propagation. In: Sibbett GS, Ferguson L (eds.). Olive Production Manual (2nd ed.). UC ANR Pub 3353. Oakland CA. p 1925. Tous J, Ferguson L. 1997. Olive growing in California. Olivae 67:1826. Tous J, Romero A. 2000. Arbosana IRTA i-43. Olint 2:135.
Tous J, Romero A. 2002. Ficha varietal de olivo Koroneiki IRTA i-38. Olint 6:235. Tous J, Romero A, Hermoso JF. 2010. New trends in olive orchard design for continuous mechanical harvesting. Adv Hort Sci 24(1):4352. Tous J, Romero A, Plana J. 1999. IRTA-i-18, a clone of the Arbequina olive cultivar. Olivae 77(6):502. Tous J, Romero A, Plana J. 2003. Plantaciones superintensivas en olivar. Comportamiento de 6 variedades. Agricultura 851(4):34650. Tous J, Romero A, Plana J, Hermoso JF. 2008. Olive oil cultivars suitable for very high density planting conditions. Acta Hort 791:4038. UC Davis Olive Center. 2009. Survey of Super High Density Olive Production in California. http://olivecenter.ucdavis.edu/files/survey%20111509%20revised. pdf. Vossen PM. 2007. Olive oil: History, production and characteristics of the worlds classic oils. HortScience 42(5):1093100.
Scientists at IRTAs Mas de Bover research station are evaluating additional clonal materials and old orchards of olive varieties, and prioritizing the search
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Olive cultivars field-tested in super-high-density system in southern Italy

California production of extra-virgin olive oil is reportedly about 2% of total U.S. consumption, with the rest imported mainly from Italy and Spain. In ccording to the International Olrecent years, California has started inive Oil Council, world olive oil creasing its oil olive acreage. California consumption has risen from 2.8 milolive growers have planted more than lion tons (1991-1992) to 3.5 million tons 22,000 acres since 1999, about 12,000 (2005-2006), due to increases in the acres of which is in the super-highconsumption of healthier foods in many density olive system, with tree densities countries, including the United States. of 676 per acre or more. This system alThe market outlook for extra-virgin ollows for mechanical planting and harive oil is very good, and many countries vesting of olives, reducing labor costs. are actively increasing their olive acreWe believe that super-high-density ages, particularly in North Africa, the olive culture can help to assure profitMiddle East, South America, Australia ability for both European and U.S. olive and the United States (Godini 2010). growers in the coming decades. This The Mediterraneans traditional olive model, born in Spain at the end of the industry is based on production sys20th century, has resulted in noticeable tems that are hundreds of years old and increases in yield per acre. Up until characterized by low yields and high now, super-high-density olive culture production costs. The European Union has utilized a limited number of cultisubsidy system, which has helped vars, primarily Arbequina, Arbosana European olive farmers to stay in busiand Koroneiki, which possess suitable features such as a semidwarf habit, early bearing (first production at the second-to-third year after planting), consistent initial crops (more than 2.2 pounds per plant), crop stabilization between 5 and 6 years, and fruit that is impact-resistant and has good oil quality (Godini and Bellomo 2002). The results that we present here are preliminary. Considering that Italys Mediterranean climate Super-high-density hedgerow planting systems for olives is similar to Californias, employ over-the-row harvesters (shown, in California). we believe that soil and ness, will end in 2014. Moreover, the climate differences should have little application of a free exchange area influence on the applicability of these in 2010 will legalize the importation of findings to California. lower-cost extra-virgin olive oils from Experimental orchard the southern Mediterranean Basin into In summer 2006, we established Europe (Godini 2010). Year after year, a new experimental orchard at the profitability of Italys traditional Valenzano, near Bari, in the experimenolive culture becomes increasingly tal farm of the Dipartimento di Scienze doubtful, notwithstanding the worlddelle Produzioni Vegetali at University wide renown of so-called Made in Italy extra-virgin olive oil (Godini and Aldo Moro of Bari, Italy. In addition to standard clones of Arbequina, Bellomo 2002).
by Angelo Godini, Gaetano Alessandro Vivaldi, and Salvatore Camposeo
Paul M. Vossen
Arbosana and Koroneiki, two additional cultivars were introduced: Coratina, the most popular Apulian olive oil cultivar, and Urano, a new Italian cultivar considered by our research group to be well-suited for super-high-density olive culture. The olive trees were propagated in commercial nurseries by softwood cutting, and the experimental orchard was established according to the super-highdensity planting scheme (676 plant per acre, with a tree spacing of 157.5 inches by 59 inches) and a north-south row orientation. The trees were trained to central leaders. Drip irrigation was supplied to each tree every 3 days between late spring and late summer, increasing from 423 cubic yards per acre annually in 2006, to 476 in 2007, to 794 in 2008 and 2009. Harvesting was performed on Nov. 20 in 2008 and 2009, in the third and fourth years after planting, respectively, using the Pellenc Activ 4560 harvesting machine.
Cultivar performance
Vegetation. In December 2009, the average tree height had reached 107 inches, 5.3 times the initial growth of the previous year, with a maximum of 7.6 times more growth for Arbequina and a minimum of 2.2 times more for Urano (table 1). Only the crown width of Coratina exceeded 79 inches by
TABLE 1. Tree height at planting (June-July 2006) and December 2009, crown width in December 2009 Crown width December 2009 77.5b 77.7b 96.5a 78.4b 74.5b 80.9
Tree height Cultivar Arbequina Arbosana Coratina Koroneiki Urano Mean Planting 14.1b* 13.0b 16.9b 16.0b 41.1a 20.2 December 2009 inches 107.3b 97.0c 120.9a 117.6a 92.7c 107.1
* Within the same column and for a single parameter, different letters mark values significantly different at P = 0.01 (SNK test).
December 2009, exceeding the harvester tunnel size and requiring pruning intervention to control its transverse canopy growth. Annual yields. The average annual yield in the third year was 7.7 pounds per tree, equivalent to 2.3 tons per acre; only Urano exhibited a surprisingly high yield of 3.7 tons per acre (table 2). In the fourth year, the average crop yield was 11 pounds per tree or 3.3 tons per acre (up 40% from 2008), and it was more variable among cultivars. Koroneiki, Arbosana and Arbequina followed by Coratina gave satisfactory yield (between 13.7 and 11.3 pounds per tree or 4.1 and 3.4 tons per acre). The yield for Urano dropped to 4.9 pounds per tree or 1.5 tons per acre, perhaps due to heavy cropping in the previous year. Cumulative yields and oil. We also compared cumulative yields over the first 4 years of the trial. Koroneiki showed the highest cumulative yield (41.3 tons per acre), and Urano was relatively less productive (31.6 tons per acre) (table 2). The peculiar behavior of Urano requires further investigation. Considering its average overall oil content of about 17.0%, Koroneiki was the most productive cultivar with 6.9 tons per acre of oil over 4 years. The other cultivars exhibited similar cumulative oil production.
Harvesting efficiency, fruit and shoot damage. Harvesting efficiency was
TABLE 2. Fruit production per year, cumulative yield at the third (2008) and fourth (2009) year after planting, and mean oil output and cumulative production Fruit production Cultivar Arbequina Arbosana Coratina Koroneiki Urano Mean 3rd year 5.5b 6.2b 7.1b 8.4b 12.1a 7.7 4th year 12.4ab 12.6ab 11.3b 13.7a 4.9c 11.0
Cumulative yield* tons/acre 33.4b 35.1ab 34.1b 41.3a 31.6c 35.1
Mean oil output % 17.7 17.5 17.3 15.0 16.8 16.9
Cumulative oil production tons/acre 5.68b 5.83b 5.86b 6.89a 5.26b 5.91
. . . . . . . pounds/tree . . . . . . .
* Over four years of the trial. 7.73 pounds per tree = 2.3 tons per acre. Within the same column and for a single parameter, different letters mark values significantly different at P = 0.01 (SNK test).
satisfactory on the whole (93.1%), notwithstanding differences among cultivars (table 3). Arbequina, Coratina and Urano had the highest harvest
TABLE 3. Harvesting efficiency, damaged fruits and damaged shoots per tree, as mean of the third and fourth year after planting Harvesting efficiency 97.2a* 87.1b 97.3a 87.6b 96.0a 93.1 Fruit damaged 0.0c 0.0c 1.5a 0.0c 0.4b 0.4 Shoots damaged n/tree 0.4b 0.5ab 0.2c 0.6a 0.2c 0.4
efficiency; Arbosana and Koroneiki were less satisfactory. But these differences were due to the fruit-ripening stages reached by each cultivar at the harvesting date: mature for Arbequina, Coratina and Urano, but immature Arbosana and Koroneiki. No damaged fruits were reported for Arbequina, Arbosana and Koroneiki, whereas Coratina and Urano exhibited very low percentages of damaged fruit. The average percentage of shoots damaged per tree by the harvesting machine beaters was insignificant at less than 1.0%. Of these damaged shoots, young and thin current-year shoots incurred the most damage (80.0%), perhaps because they were more exposed. The percentage of damaged shoots up to 1 inch in diameter was 14.3%, and to shoots thicker than 1 inch was 5.7%. Only Coratina and Urano exhibited a significant percentage of broken shoots or branches thicker than 1 inch: Coratina because of its spreading habit between rows, and Urano because of its spreading habit and thick, bending branches.
High density, high yields
We know that higher yields have been recorded elsewhere with superhigh-density olive culture; however, we consider annual yields of about 17.5 tons per acre of fruit to be satisfactory. In fact, this value, equivalent to a yield of only about 9.4 pounds per tree, would be helpful in avoiding alternate bearing and subsequent problems that could cause conflicts between vegetative growth and cropping consistency. Tree size can be controlled by pruning when they grow larger than the size of the harvester head. Our data indicates that the noted yield limit was reached by at least four out of five cultivars in just the 4th year after planting.
A. Godini is Professor, G. Allesandro Vivaldi is Ph.D. Student, and S. Camposeo is Ph.D. Researcher, Dipartimento di Scienze delle Produzioni Vegetali, University Aldo Moro of Bari, Italy. The authors wish to thank Provincia di Bari, Italy, for its financial support of this research.
References
Camposeo S, Ferrara G, Palasciano M, Godini A. 2008. Varietal behaviour according to the superintensive oliveculture training system. Acta Hortic 791:2714. Camposeo S, Godini A. 2010. Preliminary results about the performance of 13 cultivars according to the super high density oliveculture training system in Apulia (Southern Italy). Adv Hortic Sci 24(1):1620. Camposeo S, Vivaldi GA, Gallotta A, et al. 2010. Valutazione chimica e sensoriale degli oli di alcune variet di olivo allevate in Puglia con il modello superintensivo. Frutticoltura 72(6):80-83 (in Italian with summary in English). Godini A. 2010. Lolivicoltura italiana tra valorizzazione e innovazione. Frutticoltura 72(6):5269 (in Italian with summary in English). Godini A, Bellomo F. 2002. Olivicoltura superintensiva in Puglia per la raccolta meccanica con vendemmiatrice. International Congress of Oliveculture. Spoleto (Italy), April 22-23:2304 (in Italian with summary in English).
Cultivar Arbequina Arbosana Coratina Koroneiki Urano Mean
.........%.........
*Within the same column and for a single parameter, different letters mark values significantly different at P = 0.01 (SNK test).
The present data confirms and improves upon results obtained in previous experimental trials (Camposeo and Godini 2010). In terms of early bearing and yield consistency, all the tested cultivars performed satisfactorily. And in sensory evaluations, the resulting extravirgin oils had sweet typology and were well-balanced, highly fruity and ready to use (Camposeo et al. 2010).
40
REVIEW ARTICLE
Methods evaluated to minimize emissions from preplant soil fumigation

by Suduan Gao, Bradley D. Hanson, Dong Wang, Gregory T. Browne, Ruijun Qin, Husein A. Ajwa and Scott R. Yates
Many commodities depend on preplant soil fumigation for pest control to achieve healthy crops and profitable yields. Under California regulations, minimizing emissions is essential to maintain the practical use of soil fumigants, and more stringent regulations are likely in the future. The phaseout of methyl bromide as a broadspectrum soil fumigant has created formidable challenges. Most alternatives registered today are reg ulated as volatile organic compounds because of their toxicity and mobile nature. We review research on meth ods for minimizing emissions from soil fumigation, including the effec tiveness of their emission reductions, impacts on pest control and cost. Lowpermeability plastic mulches are highly effective but are generally affordable only in highvalue cash crops such as strawberry. Crops with low profit margins such as stone fruit orchards may require lowercost methods such as water treatment or targetarea fumigation. oil fumigation with methyl bromide has been used for decades in California to control a variety of soil-borne agricultural pests, such as nematodes, diseases and weeds. Major, high-value cash crops that rely on soil fumigation include strawberries; some vegetables such as carrot, pepper and tomato; and nurseries and orchards for stone fruit, ornamentals and grapevines. In California, tree and grapevine field nurseries must meet requirements of the California Department of Food and Agriculture (CDFA) Nursery Nematode
Shank application of 1,3-D is followed by a disking/rolling operation, inset, to break the shank trace and compacted soil surface.
Control Program (CDFA 2008). Without fumigants, the productivity of these cropping systems would suffer from yield losses due to diseases, replant disorders or lack of phytosanitary certification. Because of its role in depleting stratospheric ozone, methyl bromide was phased out in the United States and other developed countries as of January 2005, under provisions of the U.S. Clean Air Act and the Montreal Protocol (an international agreement). Some limited uses of methyl bromide are permitted under critical-use exemptions and quarantine/preshipment criteria, which are subject to application and approval annually. Limited to a few registered compounds, growers have turned to alternative fumigants such as 1,3dichloropropene (Telone or 1,3-D), chloropicrin (CP) and methyl isothiocyanate (MITC) generators (metam sodium or dazomet) (Trout 2006). In addition to direct toxicity, most of these alternative fumigants are also regulated as volatile organic compounds (VOCs). Some VOCs released into the atmosphere can react with nitrogen oxides under sunlight to form harmful ground-level ozone, an important air pollutant.
Regulations such as use limits and buffer zones have been used to minimize emissions and protect public and environmental health. More-stringent regulations are being developed for fumigants to reduce air emissions, especially in ozone-nonattainment areas such as Ventura County and the San Joaquin Valley (CDPR 2008; Segawa 2008). The UC Statewide Integrated Pest Management Program recently prepared a field fumigation guide for emission control, which is available on the California Department of Pesticide Regulation website (UC IPM 2009). This paper is not intended to represent or serve as a replacement for that guide, but rather to update findings on emission-reduction technologies, including projects under the U.S. Department of Agriculture Agricultural Research Service (USDA-ARS) Pacific Area-Wide Pest Management Program. We summarize extensive research on emission reduction from soil fumigation conducted over the last few years, and identify agricultural practices for minimizing fumigant emissions while achieving good efficacy. We also identify knowledge gaps and other research needs for the near future.
Factors affecting emissions
Soil fumigants are volatile chemical compounds. The purpose of fumigation is to achieve maximum control of soilborne pests, which requires an effective concentration or exposure duration and the uniform distribution of fumigants in soil. A number of processes affect the fate of fumigants after soil application (fig. 1). Fumigants are subject to partitioning into soil air, water and solid phases (most importantly, organic matter); volatilization (emission); degradation (chemical and microbial), movement in soil via diffusion; and potential leaching. Volatilization and leaching can potentially contaminate the air and water. Emission loss is a major airquality concern. To minimize emissions as well as ensure efficacy, it is necessary
Volatilization
Air
Phase (gas/liquid/solid) distribution via diffusion, sorption, etc.
Chemical & microbial degradation
Soil
Leaching
Fumigant Organic matter
Groundwater
Fig. 1. Processes affecting the fate of fumigants in soil.

350 300 250 200 150 100 50 0 0 48 96 144 192 240 288 336
Cumulative loss of 1,3-D (% of applied)
Cis 1,3-D Trans 1,3-D
Flux (mg/m2/h)
to contain fumigants in the rhizosphere Applying fumigant deeper in the soil where plant roots are present and lowers emissions by increasing fumisoilborne pests are dominant. Without gant travel time to the surface and its proper containment, more than half of interaction with soil. Increasing the fumigants applied can be lost through shank-injection depth from 12 to 24 emissions (fig. 2). Fumigant lost into the atmosphere not Fumigant lost to atmospheric emissions not only only contributes to contributes to air pollution, but also translates into air pollution, but wasted resources intended for soil pest control. also translates into wasted resources intended for soil pest control. inches (30 to 60 centimeters) resulted Soil conditions (such as texture, in a 20% or greater reduction of methyl moisture and organic matter content), bromide emissions in bare soils (Yates weather and surface barriers, and the et al. 2002). chemical properties of the fumigant can The general consensus for bare-soil all affect emissions. Generally speaking, fumigation is that emissions from drip lower emissions are expected from soils application, especially subsurface, are with fine texture, high water content, lower than broadcast-shank injections high organic-matter content and low (Gao, Trout, Schneider 2008; Wang et temperature compared to dry soils with al. 2009). This is attributable to two faccoarse texture, low organic-matter con- tors: (1) increasing soil water content tent and high temperature. Approaches decreases air pore volume (i.e., vapor to reducing fumigant emissions include diffusion) and increases the amount application methods such as equipment of fumigant partitioning in the aquedesign (injection depth), physical barous phase and (2) there are no shank riers, irrigation, soil amendment with traces (i.e., soil fractures) that can serve chemicals or organic materials and as volatilization channels. The fumitarget-area treatment. gant diffusion rate in the liquid phase Current application techniques is much slower than in the gas phase. include broadcast fumigation and Substantially higher soil water content chemigation. With standard broadcast would reduce the fumigants distribufumigation, fumigants are applied tion in soils by reducing vapor diffudirectly to the soil at a certain depth sion, reducing efficacy. Good efficacy using conventional equipment or rigs can only be ensured when the fumigant (shanks). Chemigation is injecting moves with applied water for a relafumigants into soil with irrigation watively uniform distribution (Ajwa and ter through sprinklers or drip tapes. Trout 2004). However, because fumigants are highly volatile, drip-applied fumigants near soil surfaces without 100 any barriers may still result in high B Total 1,3-D emission losses. Currently, about half of 80 Californias strawberry acreage, especially in the coastal areas, is fumigated 60 using drip application.
40
Plastic films
20
0 0 48 96 144 192 240 288 336
Time (hours)
Time (hours)
Fig. 2. Emission flux from a bare surface soil after shank injection of 1,3-dichloropropene (1,3-D) (with 2.5% inert ingredients) at an 18-inch depth into a sandy loam soil. The 1,3-D included cisand trans-isomers; the sum of the isomers volatilized over time divided by the total applied gives the cumulative emission loss.
Plastic tarping or mulching is the most commonly used practice to contain fumigants in soil and control emissions. The effectiveness of tarping on emission reduction depends largely on the chemicals characteristics and tarp permeability, and also to some extent on soil conditions. Tarping with polyethylene film was found to be ineffective
42
A company applies fumigant through drip irrigation in a strawberry field.
Plastic tarping minimizes emissions following fumigant application.
to control 1,3-D emissions, especially in relatively dry soils (Gao and Trout 2007; Papiernik and Yates 2002). However, high-density polyethylene (HDPE) tarp applied over irrigated soil can substantially lower 1,3-D emissions, due to both higher soil water content and water condensation under the film (Gao and Trout 2007). About 50% emission reduction was measured for an HDPEtarped treatment in relatively cooler fall weather conditions, compared to bare soil (Gao, Hanson, et al. 2009). Tarped treatment in pre-irrigated soil in summer may also improve pest control due to elevated soil temperatures under the tarp. Shrestha et al. (2006) observed significant reductions in weed populations due to high temperatures up to 117F under the tarp, which was partially attributed to the effect of solarization. Virtually impermeable film. Lowpermeability films, including virtually impermeable film (VIF), showed great potential in early laboratory or smallplot tests (Wang et al. 1997b). VIF has much lower permeability to most fumigants than HDPE films (Ajwa 2008). VIF is generally a multilayered film composed of barrier polymers such as nylon or ethyl vinyl alcohol (EVOH) sandwiched between polyethylene polymer layers (Villahoz et al. 2008). A number of studies have shown that VIF can retain higher fumigant concentrations than HDPE film, reducing emissions while improving efficacy, especially for weed control (Hanson et al. 2008; Noling 2002). The effectiveness of VIF in large-field applications has been difficult to ascertain because it can be
damaged during field installation, with potential changes in permeability. Recent field data confirmed that this type of film can effectively reduce emissions more than 90% (Ajwa 2008; Gao, Qin, et al. 2009). The tarp permeability did increase after field installation but was still substantially lower than that of polyethylene films (Qin, Gao, Ajwa 2008; Yates 2008). There are also concerns about damage from field installation and improper gluing materials in the VIF tarp. These potential problems, however, were not observed in a recent field trial (Gao, Hanson, et al. 2009), when a Bromostop VIF (0.025millimeter thickness) from Bruno Rimini Corp. (London, U.K.) was applied to a shank-injected 1,3-D (Telone II) field, achieving greater than 95% emission reduction. Totally impermeable film. A new type of low-permeability film, so-called totally impermeable film (TIF), was reportedly easier to install and maintain in field applications (Chow 2008; Villahoz et al. 2008). This film has even lower permeability to fumigants than some other VIFs (Ajwa 2008). For example, the mass-transfer coefficient (indicating tarp permeability to fumigants) for TIF was 0.0004 inch (0.001 centimeter) per hour for cis 1,3-D compared to 0.028 inch (0.07 centimeter) per hour for Bromostop VIF before field application, and 0.008 inch (0.02 centimeter) versus 0.106 inch (0.27 centimeter) per hour, respectively, after installation over raised beds in the field. TIF is a five-layer film incorporated with a middle layer of EVOH into a
standard polyethylene-based film (Chow 2008). Information on field emission reductions is insufficient because this film has not been made available commercially. The most recently reported research data indicated that TIF can have similar effectiveness in reducing emissions as other VIFs; but these low-permeability films can cause emission surges when the tarp is cut and after about 1 week, due to the release of high amounts of retained fumigant (Gao et al. 2010). These emission surges would increase exposure risks to workers and bystanders. To reduce the risk, the waiting period between fumigation and tarp cutting or removal should be long enough for fumigants to degrade under the tarp. VIFs can retain fumigants under the tarp, making lower application rates possible, provided that satisfactory pest control can be achieved. The low-permeability films also showed the potential to improve the uniformity of fumigant distribution up to a certain depth in the soil profile, so lower application rates than are currently used for bare soil or underneath standard polyethylene film would be possible.
Water seals and pre-irrigation
With proper management, postfumigation water seals (with sprinklers) and pre-irrigation can reduce emissions to some extent. The latter is used to achieve adequate soil moisture if the soil is dry, but not to a level that would inhibit fumigant movement/distribution in the soil profile. Water seals reduce fumigant emissions by forming a
high-water-content layer at the soil surface, which serves as a barrier preventing the fumigant from diffusing into the air (Wang et al. 1997a). Some earlier studies showed that high water content in the surface soil provided a more effective barrier to 1,3-D movement than HDPE tarping (Gan, Yates, Wang, et al. 1998). Intermittent water seals following soil fumigation have been effective in reducing emissions of methyl isothiocyanate (Sullivan et al. 2004; Wang et al. 2005) and 1,3-D or chloropicrin in the field (Gao and Trout 2007; Yates et al. 2008a). The effect is more pronounced in reducing emission peak flux, or volatilization rates from soil, by as much as 80% following fumigant application (Gao, Qin, et al. 2009). When irrigation stops, however, the emission flux tends to increase, depending on fumigant concentrations in the soil. As a result, cumulative or total emission losses may not be reduced as substantially as the peak flux. Reducing the peak flux is important because it lowers the potential exposure risk to workers and bystanders. Buffer zones are determined based on the peak emission flux. When the proper amount of water is applied, water seals do not neces-
water content in surface soil can reduce the efficacy of a fumigant to control nematodes and weeds at or near the soil surface (Hanson et al. 2008). Sequential treatment should be considered when surface pest control is a concern.
Chemical treatments
Irrigation with sprinklers forms a water seal, which minimizes emissions after fumigation.
sarily reduce fumigant concentration and distribution in the soil profile. This would hold true when only a relatively wet surface layer (up to 6 inches of soil) is maintained, and this layer should help retain fumigants in the soil. More frequent water applications appear to be more efficient in reducing emissions than fewer applications with large amounts of water. But the high
44
Soil amendments with chemicals (such as ammonium or potassium thiosulfate [ATS or KTS], thiourea or polysulfides) sprayed over surface soil are extremely effective in reducing emissions. These chemicals can react with fumigants such as methyl bromide, 1,3-D, chloropicrin and iodomethane (methyl iodide) to form nonvolatile compounds by dehalogenation (Gan, Yates, Becker, et al. 1998; Wang et al. 2000). The practicality of using these chemicals on a large field scale to reduce fumigant emissions has yet to be determined. Considerations include cost factors when large quantities of thiosulfate are needed, and potentially undesirable soil-fumigant-thiosulfate reactions. Field trials involving spraying KTS on the soil surface following fumigation revealed that this chemical can significantly reduce emissions of 1,3-D (by about 50%) and chloropicrin (by 85%) (Gao, Qin, et al. 2008). By destroying fumigant, this chemical treatment would potentially reduce the fumigant dosage at or near the soil surface, but studies showed either no effect or a limited impact on its efficacy for controlling nematodes and/or weeds (Gan et al. 2000; Gan, Yates, Becker, et al. 1998). However, strong reactions between KTS and the fumigant occurred, which resulted in a reddish-brown surface soil color and an unpleasant smell that lasted for several weeks. This reaction was not observed in a strawberry field when KTS was applied to the furrows of raised beds, most likely due to the low levels of fumigant emission measured from the furrows (Qin, Gao, Ajwa 2008; Qin, Gao, McDonald, et al. 2008). Zheng et al. (2007) indicated that the smell may have been derived from sulfur byproducts of the transformation of thiosulfate and fumigants in the soil.
Amendments and target treatments
also reducing emissions in the laboratory and some field studies. Because fumigants are readily incorporated into organic matter (Xu et al. 2003), soil with high organic-matter content was reported to produce lower emissions (Ashworth and Yates 2007). However, field data is inconclusive regarding the efficacy of adding organic amendments such as composted dairy manure right before fumigation to reduce fumigant emissions. Yates et al. (2008b) reported that a field with organic matter (composted municipal green waste) incorporated in the previous year resulted in much lower emissions than a field without the amendment but with water seals. In a field trial with relatively high fumigant application rates, manure incorporation at 5 and 10 tons per acre (12.4 and 24.7 megagrams per hectare) did not reduce emissions (Gao, Qin, et al. 2009). Similarly, a recent trial using a higher amendment rate of 20 tons per acre (49.4 megagrams per hectare) also did not show emission reduction, possibly due to reduced bulk density from too much organic material (Gao, Hanson, et al. 2009). The quantity and quality of organic matter may also determine its effectiveness in reducing emissions. High manure application rates accompanied by irrigation and/or strong surface compaction may be needed to achieve emission reduction. However, increasing the incorporation rate may be too costly to be worthwhile. The fumigation of targeted areas such as tree rows or tree sites may be applicable for orchards where replant disease is a major concern (Browne 2008). The shank application of fumigants in row-strip (shank-strip) or drip application of fumigant in tree sites (drip-spot) have been tested in fields for efficacy as well as emissions (Gao, Trout, Schneider 2008; Wang et al. 2009). These target-area treatments lower emissions by reducing the treated acreage to less than 50% (shank-strip) or 10% (dripspot), automatically reducing the total amount of fumigants applied. Applying surface sealing or water treatment can achieve further emission reduction.
Cost estimates Soil amendment with organic materiCost is important when evaluating als such as composted manure has been the feasibility of emission-reduction effective in degrading fumigants and
TABLE 1. Emission-reduction potential and cost estimates for surface sealing/treatments to reduce emissions from soil fumigation Soil-surface treatment Bare soil HDPE tarp Low-permeability tarps (e.g., VIF) Emission-reduction potential Cost (excluding fumigant) Other considerations
Reference level, often > 60% of Not estimated for field preparations such as disking total applied fumigant emissions and compaction Up to 50%, depending on soil moisture and temperature > 90%, if tarp is installed successfully 20%50%, depending on water amount and number of applications > 50% HDPE: $950$1,100 per acre (materials, ~ $500; glue, Effective in relatively moist soils $100; application, $350; cutting and removal, $100) VIF: $1,200$1,600 per acre, assuming material cost is 1.5 to 2 times HDPE, and other costs similar to HDPE < $300 per acre, depending on water price and whether grower owns or rents sprinkler system Fumigant-to-thiosulfate active ingredient ratio of 1:1 to 1:2, at $150$300 per acre Depends on application rate and material costs; commercial composted manure is $15$30 per ton Effective in almost all conditions; unclear time needed for safe tarp removal May reduce efficacy at surface soil, requiring double treatments in sequence Oversupply of nutrients to soil, post-treatment odor and potential soil-property changes Improves soil properties; consider when free or low-cost materials are available
Water treatment
Chemicals (e.g., thiosulfate)
Composted manure
Inconclusive
techniques for different commodities (table 1). Field data from a number of trials showed that low-permeability plastic tarps are the most promising technique but also the most costly. The commonly used standard polyethylene tarp costs about $950 to $1,100 per acre depending on acreage, with higher costs for small acreage and lower costs for large acreage (personal communication, industry representatives). Costly plastic materials may not be affordable for commodities with low profit margins, such as stone fruit orchards and annual vegetables. Low-permeability films such as VIF or TIF generally cost 1.5 to 2 times the cost of polyethylene films. In addition to the higher cost for VIF, high levels of fumigants may be released into the atmosphere upon removal or when planting holes are cut into the tarp. To reduce potential exposure risks, longer waiting periods between fumigation and tarp cutting/removal are necessary to allow fumigant degradation in soils. This issue requires further detailed investigation, as the fate of fumigants would vary depending on the soil and environmental conditions. If applicable, the injection of thiosulfate through drip irrigation under the tarp may effectively reduce this risk (Qin et al. 2007), although no field tests have been done. Caution must be taken when considering a chemical treatment such as thiosulfate for reducing emissions. The cost of this chemical fertilizer is low, at less than $2 per gallon (about 11 pounds) of
ammonium thiosulfate (Thio-Sul, containing 12% nitrogen and 26% sulfur). To meet crop sulfur requirements, ammonium thiosulfate is recommended at 6 to 12 gallons per acre for row and vegetable crops, and 5 to 10 gallons per acre for trees and vines using soil injection and surface banding, or 15 to 20 gallons per acre in a broadcast spray (www.tkinet.com/thiosul.html). However, fumigation rates are often much higher than fertilization rates. For example, 1,3-D can be applied at a maximum rate of 33.7 gallons (332 pounds active ingredient) per acre in California. Research showed that to significantly reduce emissions, thiosulfate and fumigant are needed at a ratio greater than one-to-one in molecular weight. For 1,3-D, a one-to-one ratio would require about 75 gallons of ammonium thiosulfate containing the active ingredient, at a cost of about $150 per acre. While this level of thiosulfate would likely reduce emissions, it could also introduce excessive nutrients or salts that cause other serious crop-production concerns. Thus, large-field applications of chemical treatment with thiosulfate are undesirable. Additional concerns with chemical treatment are the post-application odor and potential soil-property changes that have not been fully addressed. Water seals, deep injection, drip application and the incorporation of high rates of organic materials are also low-cost options to control fumigant emissions. Using water costs much less than plastic tarps and offers some
environmental benefits, because no materials must be disposed of. The cost for a 25-millimeter water application by sprinklers ranges from $100 to $300 per acre, depending on whether the grower owns or rents the sprinkler system. The overall cost of using water is currently substantially lower than plastic tarps, but this may change over time depending on water supplies in California. Commercially available, clean, composted manure costs $15 to $30 per ton. The costs to apply higher rates than 25 tons per acre may not be feasible for commodities with low profit margins. In some situations, composted green waste from municipalities may be available at no cost; however, this material may also contain other undesirable waste products, such as plastic.
Research needs
Reducing emissions from soil fumigation is required to comply with environmental regulations. Low emissions can be achieved through the management of application methods such as deep injection and subsurface drip, physical barriers with plastic films, irrigation to form water seals or achieve relatively moist soil conditions, and the reduction of treatment areas to planting rows or sites. Soil chemical treatment (e.g., thiosulfate) can be effective in lowering emissions and may prove to be an effective strategy for extreme cases, such as fumigant spills. Although the incorporation of composted dairy manure to surface soil at or
below 25 tons per acre did not reduce emissions in some field tests, the longer incorporation times and higher rates accompanied by certain soil preparations or more effective materials may have the potential to reduce emissions and improve soil physiochemical properties. Low-permeability plastic tarps such as VIF have shown the most promise in reducing emissions while improving efficacy. This type of film may also need lower application rates, which can help compensate for its high cost. Research on the performance of the next generation of low-permeability
References
Ajwa H. 2008. Testing film permeability to fumigants under laboratory and field conditions. In: Proc Ann Int Res Conf on MeBr Alternatives and Emission Reductions, Nov. 1114, 2008. Orlando, FL. p 35(1-2). Ajwa HA, Trout TJ. 2004. Drip application of alternative fumigants to methyl bromide for strawberry production. HortScience 39:170715. Ashworth DJ, Yates SR. 2007. Surface irrigation reduces the emission of volatile 1,3-dichloropropene from agricultural soils. Env Sci Technol 41:22316. Browne G. 2008. Integrated pre-plant alternatives to methyl bromide for almonds and other stone fruits. In: Proc Ann Int Res Conf on MeBr Alternatives and Emission Reductions, Nov. 1114, 2008. Orlando, FL. p 12(14). [CDFA] California Department of Food and Agriculture. 2008. Nematode Inspection Procedures Manual (NIPM). Sacramento, CA. www.cdfa.ca.gov/phpps/pe/ NIPM.htm. [CDPR] California Department of Pesticide Regulation. 2008. Ventura County fumigation emission allowances from May 1 to October 31, 2008. Sacramento, CA. www.cdpr.ca.gov/docs/emon/vocs/vocproj/emission. htm. Chow E. 2008. Properties of EVOH and TIF films for the reduction of fumigant dosage and VOC emission. In: Proc Ann Int Res Conf on MeBr Alternatives and Emission Reductions, Nov. 1114, 2008. Orlando, FL. p 38(1). Gan J, Becker JO, Ernst FF, et al. 2000. Surface application of ammonium thiosulfate fertilizer to reduce volatilization of 1,3-dichloropropene from soil. Pest Manag Sci 56:26470. Gan J, Yates SR, Becker JO, Wang D. 1998. Surface amendment of fertilizer ammonium thiosulfate to reduce methyl bromide emission from soil. Env Sci Technol 32:243841. Gan J, Yates SR, Wang D, Ernst FF. 1998. Effect of application methods on 1,3-D volatilization from soil under controlled conditions. J Env Qual 27:4328. Gao S, Hanson B, Qin R, et al. 2009. Measurement and assessment of field emission reductions. In: Proc Ann Int Res Conf on MeBr Alternatives and Emission Reductions, Nov. 1113, 2009. San Diego, CA. p 9(1-3). Gao S, Qin R, Ajwa H, et al. 2010. Evaluation of TIF to reduce fumigant emissions and the potential to use reduced rates. Ann Int Res Conf on MeBr Alternatives and Emission Reductions, Orlando, Nov 25. p 12(1-4). Gao S, Qin R, Hanson BD, et al. 2009. Effects of manure and water applications on 1,3-dichloropropene and chloropicrin emission in a field trial. J Agr Food Chem 57:542834.
films is needed for large-field applications. Any emission-reduction technology that enhances degradation or reduces fumigant concentration in soil or surface soil would have an undesirable impact on pest control because of the reduction in exposure dosage. This makes it more desirable to use low-permeability tarps, which unfortunately cost the most. Feasible techniques for different commodities depend on their availability to the production system, effectiveness in emission reduction, potential impact on pest control and cost.
Gao S, Qin R, McDonald JA, et al. 2008. Field tests of surface seals and soil treatments to reduce fumigant emissions from shank-injection of Telone C35. Sci Total Env 405:20614. Gao S, Trout TJ. 2007. Surface seals to reduce 1,3dichloropropene and chloropicrin emissions in field tests. J Env Qual 36:1109. Gao S, Trout TJ, Schneider S. 2008. Evaluation of fumigation and surface seal methods on fumigant emissions in an orchard replant field. J Env Qual 37:36977. Hanson BD, Gao S, Gerik J, et al. 2008. Pest control with California approved nursery stock certification 1,3-D treatments. In: Proc Ann Int Res Conf on MeBr Alternatives and Emission Reductions, Nov. 1114, 2008. Orlando, FL. p 25(1-4). Noling JW. 2002. Reducing methyl bromide field application rates with plastic mulch technology. Pub ENY-046, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, FL. Papiernik SK, Yates SR. 2002. Effect of environmental conditions on the permeability of high density polyethylene film to fumigant vapors. Env Sci Technol 36:18338. Qin R, Gao S, Ajwa H. 2008. Low permeable tarps reduce emissions from drip-applied inline in a strawberry field trial. In: Proc Ann Int Res Conf on MeBr Alternatives and Emission Reductions, Nov. 1114, 2008. Orlando, FL. p 114 (1-4). Qin R, Gao S, Hanson BD, et al. 2007. Effect of drip application of ammonium thiosulfate on fumigant degradation in soil columns. J Agr Food Chem 55:81939. Qin R, Gao S, McDonald JA, et al. 2008. Effect of plastic tarps over raised-beds and potassium thiosulfate in furrows on chloropicrin emissions from drip fumigated fields. Chemosphere 72:55863. Segawa R. 2008. California regulatory issues for fumigants. Presentation at Ann Int Res Conf on MeBr Alternatives and Emission Reductions, Nov. 1114, 2008. Orlando, FL. www.mbao.org/2008/004segawa.pdf. Shrestha A, Gao S, Trout TJ. 2006. Surface water applications for reducing emissions from Telone C35: Their effect on weed populations. In: Proc Ann Int Res Conf on MeBr Alternatives and Emission Reductions, Nov. 69, 2006. Orlando, FL. p 116(1-4). Sullivan DA, Holdsworth MT, Hlinka DJ. 2004. Control of off-gassing rates of methyl isothiocyanate from the application of metam-sodium by chemigation and shank injection. Atmos Env 38:245770. Trout T. 2006. Fumigant use in California response to the phase-out. In: Proc Ann Int Res Conf on MeBr Alternatives and Emission Reductions, Nov. 69, 2006. Orlando, FL. p 18(1-6).
S. Gao is Research Soil Scientist, Water Management Research Unit, U.S. Department of Agriculture Agricultural Research Service (USDA-ARS), Parlier; B.D. Hanson is Cooperative Extension Specialist, Department of Plant Sciences, UC Davis; D. Wang is Research Leader, Water Management Research Unit, USDA-ARS, Parlier; G.T. Browne is Project Coordinator, USDA-ARS Pacific Area-Wide Pest Management Program, UC Davis; R. Qin is Postdoctoral Research Associate, and H.A. Ajwa is Cooperative Extension Specialist, Department of Plant Sciences, UC Davis; and S.R. Yates is Research Leader, Contaminant Fate and Transport Unit, USDA-ARS, Riverside.
[UC IPM] UC Statewide Integrated Pest Management Program. 2009. Field Fumigation. UC ANR Pub 9005. Oakland, CA. 121 p. Villahoz MD, Garza F, Barrows P, Sanjurjo M. 2008. TIF (totally impermeable film): An innovative film for mulch, broadcast fumigation, and greenhouses in agriculture. In: Proc Ann Int Res Conf on MeBr Alternatives and Emission Reductions, Nov 1114, 2008. Orlando, FL. p 37(1-2). Wang D, Browne B, Gao S, et al. 2009. Spot fumigation: Fumigant gas dispersion and emission characteristics. Env Sci Technol 43:57839. Wang D, Juzwik J, Fraedrich SW, et al. 2005. Atmospheric emissions of methyl isothiocyanate and chloropicrin following soil fumigation and surface containment treatment in bare-root forest nurseries. Can J Forest Res 35:120212. Wang D, Yates SR, Ernst FF, et al. 1997a. Methyl bromide emission reduction with field management practices. Env Sci Technol 31:301722. Wang D, Yates SR, Ernst FF, et al. 1997b. Reducing methyl bromide emission with a high barrier plastic film and reduced dosage. Env Sci Technol 31:368691. Wang Q, Gan J, Papiernik SK, Yates SR. 2000. Transformation and detoxification of halogenated fumigants by ammonium thiosulfate. Env Sci Technol 34:371721. Xu JM, Gan J, Papiernik SK, et al. 2003. Incorporation of fumigants into soil organic matter. Env Sci Technol 37:128891. Yates SR. 2008. Update of film permeability measurements for USDA-ARS area-wide research project. In: Proc Ann Int Res Conf on MeBr Alternatives and Emission Reductions, Nov. 1114, 2008. Orlando, FL. p 18(1-4). Yates SR, Gan J, Papiernik SK, et al. 2002. Reducing fumigant emissions after soil application. Phytopathology 92:13448. Yates SR, Knuteson J, Ernst FF, et al. 2008a. Reducing field-scale emissions of 1,3-D with composted municipal green-waste. In: Proc Ann Int Res Conf on MeBr Alternatives and Emission Reductions, Nov. 1114, 2008. Orlando, FL. p 32(1-3). Yates SR, Knuteson J, Ernst FF, et al. 2008b. The effect of sequential surface irrigations on field-scale emissions of 1,3-dichloropropene. Env Sci Technol 42:87538. Zheng W, Gan J, Papiernik SK, Yates SR. 2007. Identification of volatile/semivolatile products derived from chemical remediation of cis-1,3-dichloropropene by thiosulfate. Env Sci Technol 41:64549.
46
2010 index
The following peer-reviewed research articles, and news and editorial coverage, were published in California Agriculture, Volume 64, Numbers 1 to 4 (JanuaryMarch, AprilJune, JulySeptember, OctoberDecember), 2010. Back issues are $5 per copy, while supplies last. To subscribe to the journal, order back issues, search the archives and download PDFs of all research articles in full, go to: http://CaliforniaAgriculture.ucanr.org.
JanuaryMarch, 64(1)
AprilJune, 64(2)
JulySeptember, 64(3)
OctoberDecember, 64(4)
Research and Review Articles

Animal, avian, aquaculture and veterinary sciences
Favetto PH, Hoar BR, Myers DM, Tindall J. Progesterone inserts may help to improve breeding readiness in beef heifers. 64(2):10611. SF Jinks AD, Oltjen JW, Robinson PH, Calvert CC. Fecal pats help to predict nutrient intake by cattle during summer on Californias annual rangelands. 64(2):1015. SF Richmond OMW, Chen SK, Risk BB, et al. California black rails depend on irrigationfed wetlands in the Sierra Nevada foothills. 64(2):8593. SF Van Eenennaam AL, Weber KL, Cooprider K, Drake DJ. Integrated data-collection system tracks beef cattle from conception to carcass. 64(2):94100. SF Kaiser LL, Martin AC, Steinberg FM. Research and outreach can lessen the overall burden of diabetes in farmworkers. 64(1):1721. FW Miller LMS. Cognitive and motivational factors support health literacy and acquisition of new health information in later life. 64(4):18994. AG Ober BA. Memory, brain and aging: The good, the bad and the promising. 64(4):17482. AG Sokolow AD, Varea Hammond S, Norton M, Schmidt EE. California communities deal with conflict and adjustment at the urban-agricultural edge. 64(3):1218. AL SIDEBAR: Sokolow AD, Lobo RE, Hukari K. Confined facilities create conflicts in San Diego County communities. 64(3):127. AL
Pest management
Varela LG, Walker JTS, Lo PL, Rogers DJ. New Zealand lessons may aid efforts to control light brown apple moth in California. 64(1):612. SIDEBAR: Smith RJ. National Research Council reviews pest status of light brown apple moth. 64(1):9.
Climate change issue, Cal Ag Web site, Byron win ACE awards. 64(3):117. Corrections. 64(1):5. Suckow hired as Cal Ags new art director. 64(3):117.
Outlook
Sokolow AD. Budget cuts threaten the Williamson Act, Californias longstanding farmland protection program. 64(3):118 20. AL
Plant sciences
Krasnow MN, Matthews MA, Smith RJ, et al. Distinctive symptoms differentiate four common types of berry shrivel disorder in grape. 64(3):1559. Lopus SE, Santibaez MP, Beede RH, et al. Survey examines the adoption of perceived best management practices for almond nutrition. 64(3):14954. OHara KL, Grand LA, Whitcomb AA. Pruning reduces blister rust in sugar pine with minimal effects on tree growth. 64(1):316. Shaw DV, Gordon TR, Larson KD, et al. Strawberry breeding improves genetic resistance to Verticillium wilt. 64(1):3741.
Research news
Meadows R. Aging baby boomers to challenge Golden State. 64(4):1656. AG SIDEBAR: Meadows R. Minority outreach and Alzheimers disease. 64(4):165 AG Meadows R. Sierra foothills research center celebrates 50 years of rangeland productivity 64(2):5762. SF SIDEBAR: Meadows R. Protecting rangelands from overgrazing. 64(2):59. SF Sierra Foothill Research and Extension Center: Research locations. 64(2):51. SF
Economics and public policy

Schmidt EE, Thorne JH, Huber P, et al. A new method is used to evaluate the strategic value of Fresno County farmland. 64(3):12934. AL Volpe RJ III, Green R, Heien D, Howitt R. Wine-grape production trends reflect evolving consumer demand over 30 years. 64(1):426.
Land, air and water sciences

Long RF, Hanson BR, Fulton AE, Weston DP. Mitigation techniques reduce sediment in runoff from furrow-irrigated cropland. 64(3):13540. Mangiafico SS, Newman J, Mochizuki M, et al. Nurseries surveyed in Southern California adopt best practices for water quality. 64(1):2630. Ngo MA, Pinkerton KE, Freeland S, et al. Airborne particles in the San Joaquin Valley may affect human health. 64(1):126. FW OGeen AT, Dahlgren RA, Swarowsky A, et al. Research connects soil hydrology and stream water chemistry in California oak woodlands. 64(2):7884. SF Rice EC, Grismer ME. Dry-season soil water repellency affects Tahoe Basin infiltration rates. 64(3):1418.
News departments
Editorials/editorial overviews
Allen-Diaz B. Time for reflection time for action. 64(4):162. Craigmill AL, Tate KW. SFREC research sustains rangeland and oak woodlands. 64(2):546 (overview). SF Klingborg D, Sams R. What can we do for UC today? 64(1):2. Sams RW. New strategies deliver solutions-oriented science. 64(3):114.
Human and community development

Aldwin CM, Yancura LA. Effects of stress on health and aging: Two paradoxes. 64(4):1838. AG Barrett GJ, Blackburn ML. The need for caregiver training is increasing as California ages. 64(4):2017. AG SIDEBAR: Swanson PCW, Varcoe KP. Long-term care is an important consideration in financial planning for later life. 64(4):206. AG Blackburn ML. Limited-income seniors report multiple chronic diseases in qualityof-life study. 64(4):195200. AG Blackburn ML, Gillogy B, Hauselt P. Research is needed to assess the unique nutrition and wellness needs of aging Californians. 64(4):16773. AG Block Joy A, Hudes M. High risk of depression among low-income women raises awareness about treatment options. 64(1):225.
Special issue/section key

AG = Aging AL = Agricultural land FW = Farmworker health and safety SF = Sierra Foothill Research and Extension Center
Natural resources
McCreary DD. A quarter century of oak woodland research in the Sierra foothills supports oak restoration. 64(2):638. SF Pasternack G, Fulton AA, Morford SL. Yuba River analysis aims to aid spring-run chinook salmon habitat rehabilitation. 64(2):6977. SF
Index 2010
64(1):47.
Letters
64(1):5; 64(2):53; 64(3):117.
Other news
Cal Ag art director retires. 64(2):53.
UC prohibits discrimination or harassment of any person on the basis of race, color, national origin, religion, sex, gender identity, pregnancy (including childbirth, and medical conditions related to pregnancy or childbirth), physical or mental disability, medical condition (cancerrelated or genetic characteristics), ancestry, marital status, age, sexual orientation, citizenship, or service in the uniformed services (as defined by the Uniformed Services Employment and Reemployment Rights Act of 1994: service in the uniformed services includes membership, application for membership, performance of service, application for service, or obligation for service in the uniformed services) in any of its programs or activities. University policy also prohibits reprisal or retaliation against any person in any of its programs or activities for making a complaint of discrimination or sexual harassment or for using or participating in the investigation or resolution process of any such complaint. University policy is intended to be consistent with the provisions of applicable State and Federal laws. Inquiries regarding the Universitys nondiscrimination policies may be directed to the Affirmative Action/Equal Opportunity Director, University of California, Agriculture and Natural Resources, 1111 Franklin Street, 6th Floor, Oakland, CA 94607, (510) 987-0096.
California Agriculture 1301 S. 46th Street Building 478, MC 3580 Richmond, CA 94804 [email protected] Phone: (510) 665-2163 Fax: (510) 665-3427
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Olive production manuals
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ANRs Olive Production Manual (2nd ed.) is the definitive guide to olive production in California. Notable additions to the 2005 edition include a chapter on deficit irrigation, a greatly expanded chapter on olive oil production, and coverage of four new pests, including the olive fruit fly. The manual includes production techniques for commercial growers worldwide from orchard planning and maintenance to harvesting and postharvest processing, pollination, mechanical pruning and deficit irrigation. Designed as a companion to the Olive Production Manual, the Organic Olive Production Manual includes detailed information on plant nutrition, economics, pest and weed control, management of olive wastes, converting existing orchards to organic, and organic certification and registration. Other topics include orchard site selection, irrigation needs, terrain, temperature, soil, olive fruit fly damage, and how these vary for table versus oil olive production. Olive Production Manual (2nd ed.), ANR Pub No 3353, 180 pp, $35 Organic Olive Production Manual, ANR Pub No 3505, 112 pp, $18
An agritourism operation in the Apple Hill region of El Dorado County.
First survey of California agritourism operators
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Call (800) 994-8849 or (510) 665-2195 or go to http://anrcatalog.ucdavis.edu or visit your local UC Cooperative Extension office
The pressures of urbanization and shrinking profits have led California farmers to seek alternative approaches. Agritourism can provide growers with access to new customers as well as bolster income. More than 2.4 million visitors experienced agritourism at California farms and ranches in 2008. They stayed at guest ranches in the foothills, picked peaches in the Sacramento Valley, played in corn mazes up and down the state, shopped at onfarm stands, held weddings in fields and vineyards, and participated in myriad other agriculture-related tourism activities. In the next issue of California Agriculture journal, UC researchers present results of the first statewide economic survey of agritourism operators, to better understand the goals, needs and economic outlook for the states agritourism community.
Jack Kelly Clark

California Agriculture: Growing Bigger, Better

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California Agriculture

Growing bigger, better:

Peer-reviewed Research and News in Agricultural, Natural and Human Resources

Sustainable food systems: The global picture

Growing bigger, better: Artisan olive oil comes of age

14 Understanding the seasonal and reproductive

21 Biological controls investigated to aid management

29 High temperature affects

olive fruit fly populations in Californias Central Valley

34 Mediterranean clonal selections evaluated for

modern hedgerow olive oil production in Spain

Olive cultivars field-tested in super-highdensity system in southern Italy

41 Methods evaluated to minimize emissions from preplant soil fumigation

http://californiaagriculture.ucanr.org JANUARYMARCH 2011 3

Richard Ponzio, Ellen Rilla

Land, Air & Water Sciences: Mark E. Grismer, Ken Tate,

CALIFORNIA AGRICULTURE VOLUME 65, NUMBER 1

Father doubles artichoke yields

http://californiaagriculture.ucanr.org JANUARYMARCH 2011 5

H. White joins Cal Ag, CSIT staff

A long and storied history

Alexandra Kicenik Devarenne

CALIFORNIA AGRICULTURE VOLUME 65, NUMBER 1

Campus trees yield olive oil, body-care products

http://californiaagriculture.ucanr.org JANUARYMARCH 2011 7

CALIFORNIA AGRICULTURE VOLUME 65, NUMBER 1

Olive oil in California

http://californiaagriculture.ucanr.org JANUARYMARCH 2011 9

Olive oil definitions and regulations

* European Union rating scale, 09 points. Source: Tous et al. 1997.

Fruity 3.60a 3.20a 2.70b 2.60b 2.10c 1.80c 1.70c

Bitter 6.00a 4.20b 1.70c 0.93d 0.30d 0.22d 0.20d

Pungent 4.90a 3.90b 1.90c 1.10d 0.30e 0.22e 0.20e

CALIFORNIA AGRICULTURE VOLUME 65, NUMBER 1

How to taste olive oil

CALIFORNIA AGRICULTURE VOLUME 65, NUMBER 1

http://californiaagriculture.ucanr.org JANUARYMARCH 2011 13

CALIFORNIA AGRICULTURE VOLUME 65, NUMBER 1

1998 1999 2000 2001 2002 2004

Fig. 1. Years of initial olive fruit fly detection in California counties.

Kern San Bernardino Ventura Los Angeles

http://californiaagriculture.ucanr.org JANUARYMARCH 2011 15

Alexandra Kicenik Devarenne

CALIFORNIA AGRICULTURE VOLUME 65, NUMBER 1

Jack Kelly Clark

http://californiaagriculture.ucanr.org JANUARYMARCH 2011 17

Fruit infested (%)

(B) Flies per day

Olive volume (mm3)

3,500 3,000 2,500 2,000 1,500 1,000 500

CALIFORNIA AGRICULTURE VOLUME 65, NUMBER 1

(A) Yolo 1 (n = 1,133)

(B) Solano 4 (n = 972)

(C) Butte 1 (n = 870)

Dissected females (%)

(D) Napa 1 (n = 937)

(E) San Diego 1 (n = 1,095)

http://californiaagriculture.ucanr.org JANUARYMARCH 2011 19

Managing olive fruit fly

CALIFORNIA AGRICULTURE VOLUME 65, NUMBER 1

Biological controls investigated to aid management of olive fruit fly in California

http://californiaagriculture.ucanr.org JANUARYMARCH 2011 21