ACKNOWLEDGEMENTS. Ted Batkin (Citrus Research Board) Stacy Carlsen (Marin Co. Ag. Comm.)

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1 ACKNOWLEDGEMENTS Many people have made significant contributions to the development, organization, and implementation of this conference, and they all deserve our acknowledgement and thanks for their contributions. First we wish to thank W.R. Gomes, Vice President, Division of Agriculture and Natural Resources, and Rick Standiford, Associate Vice President, DANR for their support of CCBC V. We also wish to thank the members of the CCBC V advisory planning committee for their thoughtful suggestions and contributions to the development of this conference: Ted Batkin (Citrus Research Board) Stacy Carlsen (Marin Co. Ag. Comm.) Les Ehler (UCD) Beth Grafton-Cardwell (UCR) Marshall Johnson (UCR) Andrew Lawson (CS-Fresno) Robert Luck (UCR) David Morgan (CDFA) Timothy Paine (UCR) Phil Phillips (UCCE) Michael Pitcairn (CDFA) Rick Roush (UCD) John Snyder (Riverside Co. Ag. Comm.) Dan Cahn (ANBP) Kent Daane (UCB) Larry Godfrey (UCD) Mark Hoddle (UCR) Harry Kaya (UCD) Lynn LeBeck (UCB) Nick Mills (UCB) Joseph Morse (UCR) Michael Parrella (UCD) Charles Pickett (CDFA) Jay Rosenheim (UCD) Lincoln Smith (USDA-ARS) Organizations Involved In Planning This Event Include: Agricultural Research Service, USDA Animal Plant and Health Inspection Service, USDA Association of Natural Biocontrol Producers (ANBP) California County Agricultural Commissioners California Department of Food and Agriculture (CDFA) Citrus Research Board of California The California State University System (UCR, UCD, UCB) The Center for Biological Control, UC-Berkeley The University of California System UC Division of Agriculture and Natural Resources UC-IPM Exotic Pests and Diseases Research Program UC Center for Invasive Species Research Financial Support for CCBC V was provided by: UC Center for Pest Management Research and Extension UC Division of Agriculture and Natural Resources Center for Biological Control and College of Natural Resources, UC Berkeley California Department of Food and Agriculture i

2 Citrus Research Board College of Natural and Agricultural Sciences, UC Riverside College of Agricultural and Environmental Sciences, UC Davis UC Statewide Integrated Pest Management Program Exotic Pests and Diseases Research Program of the UC Statewide IPM Program and Center for Invasive Species Association of Natural Biocontrol Producers California Agricultural Commissioners and Sealers Association Special thanks go to: This conference would not have happened without the hard work of the invited speakers and researchers who provided proceedings articles and poster contributions. Vincent D Amico III, and Geoff Attardo, the Keypoint Graphics artists, who donated the proceedings cover artwork. Lynn LeBeck, Center for Biological Control, UC Berkeley. CCBC V proceedings editors: Mark S. Hoddle, Extension Specialist in Biological Control, Department of Entomology, University of California, Riverside, CA 92521, and Marshall W. Johnson, Associate Extension Specialist & Associate Entomologist, Department of Entomology, University of California, Riverside. Backcover photograph: The Citrus Experiment Station at Riverside (University of California, Riverside Campus) circa early to mid 1930 s. This photograph was used in recognition of the centennial celebration of the Agricultural Experiment Station at UC Riverside ( ). The photograph is used with the permission of the Special Collections, University Library, University of California, Riverside. ii

3 CONTENTS I. CITRUS AND BIOLOGICAL CONTROL. YESTERDAY, TODAY, TOMORROW Notes on the Evolution of Citrus Pest Management in California Robert F. Luck The Status of Biological Control in San Joaquin Valley Citrus Elizabeth Grafton-Cardwell & Neil V. O Connell The Role of Biological Control in Citrus Pest Management in Australia Dan Papacek Diaprepes Root Weevil and Asian Citrus Psyllid: New Comers to California? Kris Godfrey and Elizabeth Grafton-Cardwell II. RISK ASSESSMENT AND WEED BIOLOGICAL CONTROL Host Specificity Testing of Weed Biological Control Agents: Initial Attempts to Modernize the Centrifugal Phylogenetic Method David T. Briese Emerging Invasive Weeds and the Potential for Biological Control...40 Joseph M. DiTomaso Risk Assessment of Ceratapion basicorne, a Rosette Weevil of Yellow Starthistle Lincoln Smith How to Best Select an Agent for Weed Biological Control Andy W. Sheppard Biological Control of Squarrose Knapweed in Northern California: a Developing Success Story?...66 Dale M. Woods & Baldo Villegas A Brief Overview of the Biological Control of Saltcedar.71 Raymond I. Carruthers, John C. Herr, Jeff Knight & C. Jack DeLoach III. URBAN FORESTRY - A TRIBUTE TO DR. DONALD DAHLSTEN Biological Control in the Urban Forest: a Tribute to Donald Dahlsten. 78 Andrew B. Lawson Biological Control of the Ash and Giant Whitefly 82 John Kabashima Chemical Ecology of Bark Beetles in California s Urban Forests 87 Steven J. Seybold, Jana C. Lee, Anna Luxova, Shakeeb M. Hamud, Pavel Jiroš, & Richard L. Penrose Biological Control of Eucalyptus Pests.95 Timothy D. Paine Elm Pests and their Management and Better New Elms for California..100 Steve H. Dreistadt & Mary Louise Flint iii

4 IV. BIOLOGICAL CONTROL IN THE URBAN ENVIRONMENT Behavioral Interactions Between Ants, Pests, and Parasitoids Implications for Biological Control Michael K. Rust and Dong-Hwan Choe Invading Terrestrial Arthropods: Overview, Pathway Analysis, and Pest Status Robert V. Dowell CityBugs: Lessons Learned Using the Internet to Answer Public Requests on Insects Vernard Lewis V. POSTER SUBMISSIONS As I was Traveling to St. Ives: the Importance of Volunteers and Networking in Biological 122 Control of Giant Whitefly T.S. Bellows, David H. Headrick, Mark S. Hoddle, Carol Meisenbacher, & Marcella Waggonner Testing for Non-Target Impacts by Gonatocerus ashmeadi and Gonatocerus fasciatus on Indigenous Sharpshooters in Southern California Elizabeth A. Boyd and Mark S. Hoddle Occurrence of Key Natural Enemies on Common Plants of North Carolina Urban Landscapes Christine Casey Bird Control in Production Strawberries with Falconry Oleg Daugovish, Michi Yamomoto, & Mathew Marrow Status of Biological Control of Tamarix spp. in California Tom L. Dudley, Peter Dalin, & Dan W. Bean Augmentation Biological Control of Arundo donax Tom L. Dudley, Adam Lambert, & Alan Kirk Successful Biocontrol of Homalodisca coagulata (Hemiptera: Cicadellidae) in French Polynesia J. Grandgirard, J. N. Petit, M. S. Hoddle, G.K. Roderick, & N. Davies Comparison of Laboratory and Ecological Host Range of the Saltcedar Leaf Beetle with Respect to Native Non-Target Frankenia Species John C. Herr, Raymond I. Carruthers, & C. Jack DeLoach Evaluation of a Biopesticide, Pichia anomala WRL-076 to Control Aspergillus flavus in a..152 Commercial Orchard Sui Sheng T. Hua, Dan E. Parfitt, & Brent A. Holtz The Effect of Floral Resources on Longevity and Fecundity of Gonatocerus ashmeadi, G. triguttatus, and G. fasciatus, parasitoids of the glassy-winged sharpshooter Nicola A. Irvin & Mark S. Hoddle On Different Wave Lengths: Courtship Acoustics of the Cotesia flavipes Complex Andrea L. Joyce, R.E. Hunt, S.B. Vinson, & J.S. Bernal Effect of Irrigation and Grape Cultivar on Egg Parasitism of Arboridia kermanshah 164 (Homoptera: Cicadellidae) by Anagrus atomus (Hymenoptera: Mymaridae) M. Kohansal, B. Hatami, J. Khajehali, & M. Mobli iv

5 V. POSTER SUBMISSIONS CONTINUED Host Specificity of the Mymarid Anagrus epos Girault, A parasitoid of Cicadellidae Eggs..168 Rodrigo Krugner, Marshall W. Johnson, Joseph G. Morse, & Russell L. Groves Parasitoid Community Ecology of Sunflower Moth in California s Great Central Valley Caterina Nerney Susceptibility of the Olive Fruit Fly, Bactrocera oleae (Diptera: Tephritidae), to.176 Entomopathogenic Nematodes Farshid Sirjani, Ed Lewis, & Harry K. Kaya Biocidal and Allelopathic Properties of Gramineous Crop Residue Amendments as.179 Influenced by Soil Temperature James J. Stapleton A Large-Scale Demonstration of Solar Inactivation of Invasive Weed Propagules for..182 Revegetation with California Native Wildflower Communities James J. Stapleton & Susan Jett Response of Phytoparasitic Nematodes and Microbial Soil Community Structure to 184 High-Temperature Tent Solarization for Disinfesting Container Nursery Soil James J. Stapleton, Megan N. Marshall, & Jean S. VanderGheynst Quantification of Powdery Mildew Consumption by a Native Coccinellid:..188 Implications for Biological Control? Andrew M. Sutherland & Michael P. Parrella Agricultural Biological Control as Public Science: an Initiative to Enhance Support for Ecological Alternatives to Pesticides in California K.D. Warner, C. Getz, S. Calderón, & S. Maurano Augmentative Biological Control in the United States: Identifying Obstacles and 196 Proposing New Strategies K.D. Warner & A. Hazlehurst v

6 Notes on the Evolution of Citrus Pest Management in California Robert F. Luck, Department of Entomology, University of California, Riverside, CA Citrus was introduced into California during the late 18 th and early 19 th Centuries by Franciscan Monks who were charged with the responsibility of establishing a Spanish presence in (Alta) California. Citrus is an exotic plant to the Western Hemisphere. It arrived in the New World from the Mediterranean region via Hispaniola (Haiti), in 1493, as seeds, when Columbus made his second voyage to the Caribbean (Webber et al., 1967). This introduction likely led to the establishment of sweet orange, sour orange, lemon, citron, and probably lime, i.e., the citrus cultivars familiar to the Spanish and Portuguese by their presence on the Iberian Peninsula in the 15 th Century. Similarly, the Portuguese introduced oranges, lemons, and citrons into Brazil around 1540 while the Spanish introduced these varieties into Argentina and the west coast of South America sometime before the middle of the 17 th Century. By 1653, sightings of citrus in Peru both sweet and sour were noted by a Spanish traveler (Webber et al., 1967). Thus, by the middle of the 17 th Century, citrus, i.e., oranges, lemons, limes, and citrons, was widely distributed in the Americas including populations of feral citrus in Florida and other tropical and semi tropical regions. However, citrus did not reach the American Southwest until 1697 (Webber et al., 1967), largely because the Spanish thought Baja and Alta California were an Island and, from their point of view, these were not as important a region to settle as was Mexico proper (Starr, 2005). Several Spanish expeditions had sailed along the California coast as far as Cape Mendocino to locate a potential port for Spanish Galleons sailing across the Pacific Ocean from the Philippines but no settlement resulted. Interest in settling California arose only when Francisco de Ulloa, who in 1539, discovered the Colorado River and its mouth at the north end of the Gulf of California. The Spanish then realized that California was not an Island but was attached to Mexico (Starr, 2005). Still, Baja and Alta California remained unsettled until 1697, some 130 years after Francisco de Ulloa s discovery. The first Spanish settlement, a mission, was established in southern Baja by the Jesuits in However, Alta California remained unsettled for some 230 years. In contrast to California, the initial Mission in Baja California led to the establishment of a series of missions that stretched through what is now the State of Sonora, Mexico, and into southern Arizona, south of Tucson. Citrus, along with other fruit trees, annual plants, and livestock, were established in the gardens and pastures at these missions. Thus, Arizona had citrus long before (Alta) California, but, in contrast to California, it did not lead to an extensive citrus industry (Webber et al., 1967). Missions were the means by which the Spanish colonized new territory by instituting a theocratic regimen at each of the missions to proselytize and civilize the Native Americans (Starr, 2005). Initially, the Spanish had made the Jesuit Order responsible for colonizing the New World. This charge changed, however, in 1759, when Juan Carlos III ascended the Spanish Throne. He became concerned with the Jesuits theocratic governance and their penchant for political autonomy. Thus he expelled them from Mexico in 1765 and reassigned the responsibility for settling and proselytizing the Native Americans in Alta California to the Franciscan Order. This led to the establishment of a series of missions along California s coast, the first of which was Mission San Diego de Alcala, established in All tolled, 21 missions were founded, each a days ride apart. The last of these missions, founded in 1823, was Mission San Francisco Solano in Sonoma, about 100 miles north of San Francisco (Starr, 2005). All of these missions had extensive gardens and herds of livestock. Although they were religious institutions, they were also working rancheros, since they had to be self sufficient. They used the local Native Americans as their labor force, often coercively, and citrus was a part of the plantings in most of these missions. Citrus was probably included because it was an important source of vitamin C and warded off scurvy, a fatal disease resulting from a deficiency in this vitamin. It is likely that the Spanish realized that consuming citrus fruits protected them from this disease because of their sailing heritage, although they did not understand its basis. In contrast to the planting of a few citrus trees at most of the missions, three had more extensive citrus plantings: Mission Buenaventura, (Ventura CA), Mission San Gabriel Arcangel (9 miles east of downtown Los Angeles) and Mission San Luis Rey (northern San Diego County). In addition to the missions, the Mexican Government also established several Presidios (Monterey and San Francisco) and chartered two Pueblos (San Jose, next to a small creek at the south end of San Francisco Bay, and Los Angeles, nine miles west of Mission San Gabriel Arcangel along the Los Angeles River) (Starr, 2005). Ironically, a year after the founding of the last mission in Sonoma, Mexico gained its independence from Spain and became secular, as did the California Missions, although they remained as parish churches. The missions no longer had a governmental responsibility, i.e. served as a civil authority (Starr, 2005). Three citrus varieties were recorded as having been grown at the Spanish missions, the Valencia along with lemons and citrons. The first of the orange groves was planted at Mission San Gabriel around 1803 and consisted of about 400 trees established with seeds from Mission San Rafael, Baja, California. The source of the lemons and citrons is unknown but they were most likely obtained as seeds from one of the Baja California missions (Webber et al., 1967). Interestingly, some of the trees from this grove survived into the 20 th century (Webber et al., 1967). Although the missions were reluctant to provide citrus seeds or seedlings to establish groves before their secularization, dooryard citrus was common in the early 1800 s, as many of the haciendas in Los Angeles had citrus trees planted for home use in their gardens and courtyards. These had been started as seeds or seedlings obtained from the mission. The first secular grove was established in 1834 by a Frenchman, Jean Louis 1

7 Vignes, who obtained large sweet orange seedlings from Mission San Gabriel, that is, after the Mission had been secularized. These seedlings were planted on Aliso Street in Los Angeles (Webber et al., 1967). A second grove was established in Los Angeles in 1841 by William Wolfskill, a Kentucky trapper who had come overland to Los Angeles in He petitioned the Mexican government for land in Los Angeles, which it granted. He then planted and experimented with citrus production using the sweet orange seedlings he had obtained from Mission San Gabriel, eventually planting a small grove in His property was located near the old Santa Fe railroad station between the Los Angeles River and what is now 4 th and 6 th street in downtown Los Angeles. This grove was the first to be planted for profit. Wolfskill gradually learned how to grow citrus and slowly expanded his grove, eventually reaching a size of about 70 acres. His timing in developing his grove could not have been better: it was in full production when the gold rush began in He was able to sell all of his oranges to the miners. After the gold rush subsided he continued to produce citrus. The last crop on the trees sold for $25,000 before his death in He also planted the first table grape vineyard in California on a separate piece of property and also shipped these to the gold country (Webber et al., 1967). However, it was Mexico s ceding of California to the United States in 1848, a consequence of losing the Mexican American War, coupled with the discovery of gold in northern California the following year that spurred commercialization of California citrus. The discovery of gold caused a rapid increase in the population of miners and citizenry in San Francisco, Sacramento, and the gold fields in the Sierra Nevada foothills. In 1847, the non native population in California was less than 10,000; but it had swelled to 350,000 by 1850, the majority of which lived in northern California (Starr, 2005). This created a market for citrus and fruit that was shipped from Los Angeles by ocean freight via the San Pedro harbor to San Francisco and then by boat up the Sacramento, American, and Feather Rivers to the gold fields (Weber et al, 1967). Citrus was in high demand, selling for a dollar a fruit in San Francisco, and perhaps a bit more in the gold fields. Its demand was probably, in part, due to its ability to prevent scurvy. However, southern California s small citrus industry was unable to supply the huge demand for this fruit. Most of the citrus fruit entering California, some three million oranges, came from Mexico, Hawaii, and Tahiti (Webber et al., 1967). Even so, citrus planting manifested a small increase during this period and two additional groves were established in Los Angeles during the early 1850 s. One of these groves was established from seedlings shipped from Central America and Hawaii to minimize the time it took the grove to bear fruit (Weber et al., 1967). This was a major change in the method of establishing a grove, since up to this point all of the citrus plantings had been from seeds or seedlings initiated with seeds, mostly from local sources. This was necessitated by the length of time and rigors of sea transport via sailing vessels and these conditions were too uncertain to obtain a few seedlings reliably. Also, by 1857, citrus had expanded into the Inland Empire where another two groves were established in the San Bernardino-Highland area (near Riverside). The success of these groves spurred further plantings in this district, since it was clear that citrus could also be grown in the inland valleys of southern California. This further stimulated the nursery industry to supply seedlings for the expanding industry. According to the United States Department of Agriculture, 17,000 orange trees and 3,700 lemon trees were being grown in California in 1867 with 15,000 orange and 2,300 lemon trees occurring in the Los Angeles region. Citrus production continued to be stimulated during the s. Its growth was facilitated by changes in technology and transportation that occurred during this period: With the development of ocean going steamships, transportation was less rigorous and more dependable than the ocean going sailing vessels pre 1860 s (Tate, 1986). This allowed the dependable shipment of plant material. However, the greatest stimulus for the growth of California s citrus industry came with completion of a transcontinental railroad (Central Pacific and Union Pacific railroads) between Sacramento, California, and Omaha, Nebraska, in 1869, coupled with the subsequent completion of the Southern Pacific Valley Railroad Line in This latter railroad connected southern California with the transcontinental railroad in central California, which allowed growers to ship citrus by rail from southern California to northern California and then to the Eastern U.S.A. When the southern rail routes to the eastern U.S. were completed in 1881 (Southern Pacific Railroad) and 1885 (Santa Fe Railroad), they fostered price competition which stimulated citrus production further. The first shipment of citrus, destined for Saint Louis, was made from the Wolfskill Orchard in Los Angeles in 1877 and these oranges arrived in good condition after a month in transit. The first train filled exclusively with oranges, left Los Angeles for the eastern U.S., February, The successful opening of an eastern market for citrus further stimulated citrus plantings, which rose from 25,000 trees in 1862 to over a half a million orange trees in This pattern of increase continued until WW II, when the migration of labor to Los Angles for the war effort (WW II) led to the urbanization of citrus land in the San Fernando Valley (Weber et al., 1967). This was the first decline in southern California citrus production and portended the post war decline of southern California s citrus industry as urbanization of southern California burgeoned during the later half of the 20 th century. A second factor increasing the demand for citrus fruits was the development of new citrus varieties (Weber et al., 1967), particularly the Washington Navel, which was first planted in Riverside, California. The Riverside colony, founded in 1870, planted its first citrus trees in 1871 and its first Washington navel, a sweet, seedless, easy peeling fruit, in This variety matures during the winter and early spring; just in time for the late winter-early spring market in the eastern U.S. Ten years after establishing the Riverside Colony, 17,038 oranges trees were growing in the Riverside area and most of the fruit from these trees were being shipped to markets in the eastern U.S. (Webber et al., 1967). 2

8 The increasing demand for citrus also stimulated changes in the methods used to establish groves. The vast majority of citrus trees planted prior to had been established as seedlings from seeds, or from fruits with seeds, that had been imported from Mexico, Hawaii, and Tahiti, or, in the case of the Navel Orange, as seedlings from Bahia, Brazil, via Washington D.C., where the seedlings were grown before they were sent to Riverside (Webber et al., 1967). With an increasing demand for citrus, however, private nurseries developed which received new orange varieties as seedlings or young trees shipped directly from many of the citrus growing regions of the world without inspection or quarantine. The individuals establishing these nurseries were unaware of the potential for pest problems. Such seedlings would be incorporated into the nursery stock along with the pests they harbored. While there were entomologists in the U.S. at the time, they were few in number and mostly systematists located in the eastern U.S. (Howard, 1930; Compere, 1961; Doutt, 1964). Thus, the citrus growers in southern California were unaware of the potential for importing pests and this ignorance unwittingly began a period in which they imported a series of arthropod pest problems with which we live with today. The first commercial nursery in California was established in 1865 by Thomas A Garey in Los Angeles. Garey supplied trees to a number of locations that were establishing new groves through out southern California (Compere, 1961). He imported and introduced a large number of citrus varieties (and other fruit vines and trees) between 1868 and 1875, receiving shipments of citrus varieties (seedlings and seeds) from Mexico, Central America, Australia, southern Europe, and Florida, as well as from other nurseryman e.g. England, who likely obtained their stock from the British Colonies, e.g., South Africa, the Mediterranean region, the Middle East, India, and southern China (Webber et al., 1967; Compere 1961). Other southern California growers were also likely to be receiving seedlings from elsewhere. This was also the era when a number of serious arthropod pests became established in the Los Angeles citrus district and Garey s nursery was one of several sources responsible for spreading some of these pests among the citrus growing districts in southern California (Compere, 1961). Most of these pests were homopterans, which tend to be cryptic, largely sessile, and often parthenogenetic, i.e., they reproduced without having to mate. Nor did they look like insects to the naive observer. But they had the potential to ruin fruit production and to kill trees, making citrus production uneconomic. The number of exotic pests proliferated during this period and they threatened to annihilate California s young citrus industry (Doutt, 1958; Caltagironi and Doutt, 1989; Compere, 1961; DeBach and Rosen, 1991). The first pest to emerge as a threat to the industry was the cottony cushion scale, Icerya purchasi Maskell (Coccidae: Margarodidae), which reeked havoc on the industry and threatened its annihilation (Smith and Basinger, 1947; Doutt, 1958; Compere, 1961). In 1868, a California nurseryman or several nurserymen in San Mateo County imported lemon trees (Issac, 1906) and/or acacia trees (DeBach and Rosen, 1991) from Australia. The cottony-cushion scale has a number of hosts; including acacia, mock orange (Pittosporum spp.,) and citrus (Quezada and DeBach, 1973; DeBach and Rosen, 1991). A Los Angeles nurseryman and florist secured a few of these trees to introduce into Southern California (Issac, 1906) but no one noticed or was concerned about a few white, fluted, and waxy things on the wood and leaves of these plants. It was this or a similar introduction that established cottony-cushion scale in Thomas Garey s Los Angeles nursery. The scale was first detected by George Compere, Harold Compere s father, in 1878, on a few trees in Garey s nursery, the largest nursery in southern California (Compere, 1961). Also a smaller nursery occurred next to Garey s nursery in Los Angeles and Garey had a nursery inland as well (Compere, 1961). These nurseries spread this scale to other groves throughout southern California when they supplied growers with trees to expand established groves or to establish new groves. Unwittingly then, these introductions rapidly spread the scale throughout southern California s citrus growing regions (Compere, 1961). These nurseries, however, were not the only sources of the scale s introduction as the scale was subsequently detected in a Santa Barbara grove two years later by J. H. Comstock, a systematist with the U.S. Department of Agriculture, Washington D. C., while he was on a scale collecting trip to California and Utah in 1880 (Compere, 1961). By 1886, it was clear that this scale was devastating California s young citrus industry. It inhibited tree growth and fruit production and, when trees became heavily infested, it killed them (Doutt, 1968). By the late 1880 s, growers were becoming desperate, as many of them were forced to abandon citrus production entirely and at a great financial loss (Doutt, 1964). They tried a number of tactics to stop the scale s spread such as uprooting and burning infested trees, treating infested trees with oil, and tenting and fumigating trees with hydrogen cyanide (HCN) gas. None of these tactics worked. In desperation, the growers invited C.V. Riley, the Entomologist from the U.S. Department of Agriculture s Division of Entomology, to address them at the California State Fruit Grower s Convention in Riverside, April, 1887, about possible solutions to the cottony cushion scale problem. Riley recommended that the scale s natural enemies be introduced into southern California to control it. Riley had corresponded with Australian entomologists and learned that the scale was present in Australia, but it was rare. Based on this correspondence and his practical experience, C.V. Riley sent Albert Koebele to Australia to collect the scale s natural enemies. In August 1888, Albert Koebele sailed from San Francisco for Australia while, D.W. Couquillet remained in Los Angeles and built a cage around a scale-infested citrus tree in anticipation of receiving the natural enemies. The cage was to be used to propagate the natural enemies that Koebele sent back. Koebele s first shipment, consisting of 28 adult ladybird beetles, arrived November 30, Two more shipments followed during the next two months, bringing the total number of Vedalia beetles introduced into southern California to 129 adults. These beetles were propagated in the cage 3

9 and the beetle s progeny were periodically liberated and distributed throughout southern California (Smith and Basinger, 1947; Compere, 1961; DeBach and Rosen, 1991). By the following June (1889), more than 10,000 adult beetles had been distributed throughout the infested citrus areas of southern California. Also Koebele had discovered a fly, Cryptochetum iceryae (Williston) (Diptera: Cryptochetidae), associated with the scale and sent about 12,000, pupae to Couquillet. Interestingly, there is no record of this fly being recovered in southern California following it release. There is reason to believe that the fly s establishment was due to the effort of. W.G. Klee, the California State Inspector of Fruit Pests. He had been corresponding with Maskell in New Zealand and with Frazer Crawford in Australia. Maskell informed Klee that Australia was the native home of the scale and based on this correspondence, Frazer Crawford sent Klee some Cryptochetum which were liberated on cottony cushion scale in San Mateo Co. near San Francisco, in late 1888, before Koebele had set sail for Australia. Regardless of the source of the natural enemies, the outcome was spectacular. In fact, it is hard to think of how one could design a more dramatic validation of a pest suppression tactic. In a little more than a year after releasing the lady bug, the scale was gone from the trees previously infested throughout most of the infested regions in southern California. The orange shipments from Los Angeles County nearly tripled the year following the beetles release, increasing from 700 to 2000 box cars. It is likely that Klee s release of the fly in northern California resulted in its establishment (DeBach and Rosen, 1991). During the crisis, two other pest suppression tactics were developed which subsequently influenced pest management of citrus and other tree crops for decades. The first of these was HCN fumigation for California red scale, Aonidiella aurantii (Maskell), (Homoptera: Diaspididae), developed by Couquillet with the help of Alexander Craw, the foreman of J.W. Wolfskill s ranch in Los Angeles (Doutt, 1958). A canvas tarp was placed over a tree and HCN gas was pumped inside and left for a time. This tactic subsequently evolved (Quayle, 1938) and was used until the late 1950 s in some of the citrus groves of Ventura Co., California (Graebner, 1982). Also oil sprays were also used but their acceptance required considerable research and development including the spray equipment to apply them before the oils where widely accepted (Quayle, 1938). Oils continue to be used but on a more limited basis and this tactic now employs a highly refined product (e.g. Beattie et al., 2002). Cottony-cushion scale suppression by introducing its co-evolved natural enemies also validated the use of biological control as a pest control strategy, as first advocated by C.V. Riley (Doutt, 1958). Interestingly, although two natural enemies were imported and released in California for its control, the vedalia beetle got the lion s share of the credit. Its rapid increase and visibility made its work much more obvious. Cryptochetum iceryae, also introduced into California (DeBach and Rosen, 1991), largely went unnoticed. Most of fly s development is hidden from view while it is attacking the scale. The fly s maggots feed inside the immature stages of the scale and cannot be seen. Thus, its role in suppressing cottony cushion scale was largely unappreciated until the studies of Quezada and DeBach (1973) and Thórarinsson (1990 a, b), some ninety years later. These workers documented the fly s importance, especially in the cooler climates or winters in California. C. iceryae is a facultative, gregarious internal parasitoid. The number of eggs it lays on a scale larva depends on the host larva s size: the larger the larva the more eggs it lays and the more flies mature. Thus, its increase can be rapid with its short generation time. Prasad (1989) experimentally confirmed the ability of the fly and the Vedalia beetle to suppress cottony-cushion scale in Australia, their area of endemicity During the period in which cottony-cushion scale emerged as a pest, several other homopteran pests appeared around the same time period, including California black (= olive) scale, Saissetia oleae (Olivier), (Homoptera: Coccidae), California red scale, Aonidiella aurantii Maskell (Homoptera: Diaspididae), yellow scale, Aonidiella citrina Coquillett (Homoptera: Diaspididae), and several mealybugs (Homoptera: Pseudococcidae). Each of these pests represented different challenges to their suppression. The importation and establishment of natural enemies for their suppression also formed a foundation for a sustainable pest management program in southern California citrus, (Graebner, 1982; DeBach and Rosen, 1991) and, more recently, for a program being developed for San Joaquin Valley citrus (Haney et. al., 1994; Luck et al., 1997; Morse and Luck, 2003). One of the pests, California red scale, became the most serious pest after cottony-cushion scale s suppression; however, its suppression occurred bit by bit and involved a sequence of natural enemies introduced over a 90 year period with about a forty year hiatus due to poorly understood systematics of one of its major parasitoid complex, the genus, Aphytis (DeBach and Rosen, 1991). Red scale first came under control along the southern California coast while its suppression in the hotter, more interior regions of southern California came much later, during the early 1960 s. The successful suppression of the scale in the more interior region was the result of a detailed biosystematics study by DeBach and his students and it underscores the need and the value of detailed systematics and ecological research (Rosen and DeBach, 1979). This research forms the foundation for such biologically-based control. Ironically, Harold Compere, after spending a lifetime of exploring for California red scale parasitoids almost everywhere red scale occurred, became pessimistic about the possibility of red scale s suppression by natural enemies (Compere, 1961). In 1961, nearing the end of his career, he authored an article in the journal, Hilgardia, in which he reviewed the history of biological control research (and politics) surrounding this scale. In the second paragraph of this article he states that This paper expresses a pessimistic view of the possibilities for biological control of the red scale. (Compere 1961, p 173). Ironically, in , concurrent with Compere s finalizing and submission of his manuscript I suspect, DeBach had collected several colonies of a red scale parasitoid from India and Pakistan, later described as Aphytis melinus DeBach (Hymenoptera: Aphelinidae). It was this parasitoid species that finally suppressed California red scale biologically in the more 4

10 interior regions of southern California. It also formed the basis of an augmentative biological control program initially developed by Harold Lorbeer (1981) for the Fillmore Protective District in Ventura County in conjunction with several UC Riverside biological control specialists (Graebner, 1962; Graebner et al., 1984). In collaboration with Harry Griffith of ERI, Dan Marino and Luck, we tested the hypothesis that augmentative releases of A. melinus produced in a commercial insectary (ERI) were capable of suppressing red scale at subeconomic densities in a lemon grove in interior southern California (Moreno and Luck, 1992). It did! Although red scale remains a pest in San Joaquin Valley citrus, it can be suppressed augmentatively, using releases of A. melinus, if sustainable IPM is practiced (Luck et al., 1997). Such suppression costs less than an insecticidebased program but it requires a detailed understanding of the pest complex, its phenology and dynamics, and the ecology of its associated natural enemy complex (Rosen and DeBach, 1979; especially pg 49-79; DeBach and Rosen, 1991; pg ; Graebner, 1982; Haney et. al., 1994; Luck et al., 1997; Morse and Luck, 2003). Unfortunately, pesticides always seems to be the easy way out for managing this pest, but history shows that sooner or later one or more of the residents in a grove develop resistance which begins to amplify the pest problems leading to a pesticide treadmill (e.g. Luck et al., 1971; DeBach and Rosen, 1991) California red scale was inadvertently introduced into California on six lemon trees brought by Matthew Keller from Australia in According to Coquillett, these lemon trees were planted in a Los Angeles orange grove (Compere, 1961). However, evidence exists that red scale was known before An 1877 report by a committee of The Southern California Horticultural Society stated that they only knew of one location where a few trees were infested with the red scale bug (Compere, 1961). Red scale was described by the Australian taxonomist, W.H. Maskell, in 1879 and specimens obtained from Maskell by J.H. Comstock, a specialist on scale insects with the U.S. Department of Agriculture, convinced him that the red scale in California was the same as that described by Maskell in Australia (Compere 1961) However, there was a disagreement as to whether this scale species was one species or two (Compere, 1961). A difference of opinion had arisen between the taxonomists, especially those who were familiar with the field ecology of the two scales. The field workers familiar with the scale s field ecology argued that there were two scale species or strains because each strain had a distinctly different effect on the citrus trees it infested. Yellow scale only infested the leaves and fruit and was not known to kill trees, whereas red scale also attacked the trunk and branches, as well as the leaves and fruit, and it was known to kill young trees (Compere, 1961). Of the scale material that Comstock had collected during his trip to Utah and California, he had either failed to detect a difference between red (A. aurantii) and yellow scale (A. citrina [Couquillet]) or had failed to collect specimens of yellow scale. During the next fifty years, the distinction between the two scales was argued over but never resolved until a consistent morphological character was detected on the ventral side, anteromedianly, on the adult red scale but which was absent in the adult yellow scale. Finally, yellow scale was recognized as a distinct species and recognized as such unambiguously, i.e., as Aonidiella citrina (Coquillett) (McKenzie, 1937). That these two entities are species has subsequently been confirmed by Marino et al. (1972). Each of the scale species emits a pheromone that attracts its males but not those of other species (Marino et. al., 1972); thus, they are reproductively isolated. These findings resolve a disagreement that lasted some 100 years. In the late 1800 s two species of natural enemies were introduced against these two armored scales. Rhyzobius (= Lindorus) lophanthae (Blaisdell) (Coleoptera: Coccinellidae) introduced by Koebele in 1892 along with the Vedalia beetle (DeBach and Rosen, 1991), and a second coccinellid, Orcus chalybeus (Bdvl.) (Coleoptera: Coccinellidae), the steel blue lady beetle, introduced and established in Santa Barbara Co., California, in 1892 (DeBach and Rosen, 1991). A third species, Aphytis chrysomphali (Mercet) was established sometime before 1902 accidentally (DeBach and Rosen, 1991) (probably along with some infested nursery stock or seedlings). This Aphytis species is parthenogenetic; that is it does not require mating to produce offspring thus is not so surprising that it was introduced fortuitously. Subsequently, it was mass reared and widely distributed in California, but it remained a sometime effective parasitoid of red scale, but only along the southern California coast. The degree to which the California red scale was controlled by its natural enemies was negligible for the next 60 years. The degree of suppression of this scale is now substantial in the southern California s inland areas but it requires augmentation most years in the San Joaquin Valley. Four species of parasitoids are responsible for the degree of control in southern California: Aphytis lingnanensis Compere (Hymenoptera: Aphelinidae) introduced from southern China in , remains dominant in some coastal regions; Aphytis melinus DeBach (Hymenoptera: Aphelinidae), imported from India and Pakistan in , is the dominant parasitoid in the more inland areas of southern California; Comperiella bifasciata Howard (Hymenoptera: Encyrtidae), imported from southern China in 1941 and complements A. melinus in the interior; and Encarsia perniciosi Tower (Hymenoptera: Aphelinidae), imported from Taiwan in 1949 which complements A. melinus in the coastal inland areas of southern California (Yu et al., 1990). But the ability to exploit these natural enemies depended on an understanding of the parasitoids biosystematics (Rosen and DeBach, 1979) and an ecological understanding of how these parasitoids exploit these scales as hosts (Luck and Podoler, 1985; Yu et al., 1990). Coupled with a means of mass-producing the parasitoid inexpensively (DeBach and White, 1960), augmentative biological control became feasible (Lorbeer, 1981). An integrated pest management (IPM) approach involving augmentative biological control has great practical value to the management of California s citrus pests. This can be seen in the response by a group of citrus growers who formed the Fillmore Citrus Protective District in 1922 (Graebner, 1982; Graebner et al., 1984). This district was organized to spread the 5

11 cost of pest management among its grower members and thereby reduce each grower s individual costs for pest management while increasing the reliability of pest management through its use of natural enemies. Thus, it is the cost-effectiveness of the entire program that is the important criterion for judging its success, not the cost of controlling an individual pest (Graebner, 1982; Graebner et al., 1984). For example, in the decade between 1971 and 1980, the average Protective District grower spent $71.88 per hectare annually for pest control. This contrasted with the average pest control costs of $ annually for a nonmember orange grower in the same Ventura county location but who does not belong to the district. Even more dramatic in the decade encompassing the 1980 s, a member grower paid $32.50 in assessment fees as a member of the district and paid an additional $60 per hectare for the control of various pests such as weeds, ants and brown-rot (a fruit rot, Phytophthora spp.) (Weppler 1998). This was the case even though it involved the production of a soft scale parasitoid, Metaphycus helvolus (Compere), to control black scale, Saissetia oleae (Olivier) (Homoptera: Coccidae), is more expensive to produce for release than is a single pesticide application for the scale, as judged by the market price for this parasitoid if ordered from a commercial insectary (Crenshaw et al., 1996). Thus the $92.50 spent by a grower member for pest control during the last year of the decade was substantially less than the decade average paid by the non-member grower ($ per hectare). This difference in pest management cost arises from the disruptive nature of the pesticide applications for black scale and California red scale suppression. The application of broad spectrum pesticides disrupts the efficacy of the natural enemies, which then requires additional pesticide use. Thus, it is the total pest management cost for economic suppression of the pest complex that is the criterion for judging the efficacy of a pest management strategy, not the cost of producing a particular natural enemy or the cost of suppressing a particular pest species. Many pest management researchers and practioners will tend to dismiss the Fillmore Citrus Protective District s results as unique to this specific crop and/or locality and assume that it has little applicability to other situations or can be adapted to other locations. While the particular solutions discussed above are specific to a certain location or region, such thinking misses the point. It is more widely applicable as we have shown to be the case in the San Joaquin Valley (Haney et. al., 1994; Luck et al., 1997; Morse and Luck, 2003; Luck and Forster unpubl data). I find it surprising how often a grower or a practioner uses of an economic argument to justify a pesticide application yet fails to evaluate the overall cost of the management program that it will obligate him too. Who says man is an economical animal? It is clear from the history of citrus pest management that, in California, a sustainable pest management program can be developed that utilizes natural enemies as the foundation. But it also requires continued research of both a fundamental nature as well as applied research. This has been a major lesion in the evolving pest management program for citrus. It is discouraging however to see how often we have to relearn this lesson. REFERENCES Beattie, G.A.C., Watson, D.M., Stevens, M.L., Rae, D.J., Spooner-Hart, R.N Spray Oils Beyond 2000: Sustainable Pest and Disease Management. Conference Proceedings, Oct Univ. Western Sydney Publ. 627 pp. Caltagironi, L.E., Doutt, R.L The history of the vedalia beetle importation to California and its impact on the development of biological control. Ann. Rev. Entomol. 34, 1-16 Compere, H The red scale and its insect enemies. Hilgardia 31(7), Crenshaw, W., Sclar, D.D., Cooper, D A review of 1994 pricing and marketing by suppliers of organisms for biological control of arthropods in the United States. Biol. Control. 6, DeBach, P., Rosen, D Biological Control by Natural Enemies. Cambridge University Press. Cambridge. DeBach, P. White, E.B Commercial mass culture of the California red scale parasitoid, Aphytis lingnanensis. Calif. Agr. Expt. Sta. Bull pp. Doutt, R.L Vice, virtue and the Vedalia. Bull. Entomol Soc. Am. 4, Doutt, R.L The historical development of biological control. Pp In: P. DeBach (ed.), Biological Control of Insect Pests and Weeds. Chapman Hall Ltd., London. Graebner, L.A An Economic History of the Fillmore Citrus Protective District. Ph.D. Dissertation. Univ. of Calif. Riverside. 228 pp. Graebner, L.A., Moreno, D.S., Baretelle, L.L The Fillmore Protective District: a success story in integrated pest management. Bull. Entomol. Soc. Am. 30, Haney, P.G., Luck, R.F., Morse, J.G., Amon, R Energy and economic costs of insecticide application in California citrus Orchards. Proceed Internl So Citriculture VII Internl Citrus Cong., March 8-13, Acireale, Italy, 3, Howard, L.O Report of the parasites of the Coccidae in the collection of this Department. U. S. Dept. Arg. Report of the Entomologist for 1880, Howard, L.O A History of Applied Entomology. Smithsonian Misc. Coll pp. Issac, J Bugs vs. Bugs. W.W. Shannon, Superintendent of State Publishing, Sacramento CA. Lorbeer, H Integrated biological control in Fillmore citrus groves. Calif. Citrograph. 56(6),

12 Luck, R.F., van den Bosch, R., Garcia, R Chemical insect control -- A troubled pest management strategy. BioScience 27, Luck, R.F., Forster, L.D., Morse, J.G An ecologically based IPM program for citrus in California's San Joaquin Valley. Proceed Internl Soc Citriculture VIII Internl Citrus Congr., May 12-17, 1996, Sun City, South Africa. 1, Luck, R.F., Podoler, H Competitive exclusion of Aphytis lingnanensis by A. melinus: potential role of host size. Ecology 66, Luck, R.F., Forster, L Quality of Augmentative Biological Control: a Historical Perspective and Lessons Learned from Evaluating Trichogramma. In: J.C. van Lenteren, (ed.), Quality Control and Production of Biological Control Agents. Theory and Testing Procedures. CABI Publishing. CABI International. Wallingford, Oxon, U.K., pp McKenzie, H.L Morphological differences distinguishing California red scale, yellow scale, and related species. Calif. Univ. Pubs Ent. 6(13), Moreno, D.S., Rice, R.E., Carman, G.E Specificity of the sex pheromones of female yellow scale and California red scales. J. Econ. Entomol. 65, Moreno, D.S., Luck, R.F Augmentative releases of Aphytis melinus (Hymenoptera: Aphelinidae) to suppress California red scale (Homoptera: Diaspididae) in southern California lemon orchards. J. Econ. Entomol. 85, Morse, J.G. Luck, R.F The history of integrated pest management of citrus in California. Proceed IXth Internl Society of Citriculture. 5-7 December, 2000, Orlando Florida, 2: Prasad, Y.K The role of natural enemies in controlling Icerya purchasi in South Australia. Entomophaga 34, Quayle, H.J Insects of Citrus and other Subtropical Fruits Comstock Publ Co., Inc., Ithaca, New York. Quezada, J.R., DeBach, P Bioecological and population studies of the cottony-cushion, Icerya purchasi Mask, and its natural enemies, Rodolia cardinalis Mul. and Cryptochaetum iceryae Will., in southern California. Hilgardia 41, Smith, H.S., Basinger, A.J History of biological control in California. 70 th Anniversary Issue, California Cultivator. Oct. 25, pp Starr, K., California - A History. Modern Library Chronicles, Random House, Inc. New York. Thórarinsson, K Biological control of the cottony-cushion scale: Experimental tests of the spatial density dependent hypothesis. Ecology 71, Thórarinsson, K Parasitization of the cottony-cushion scale in relation to host size. Entomophaga 35, Tate, E.M Transpacific Steam. Cornwall Books, New York. Weppler, R.A Studies on the rearing of Metaphycus helvolus (Compere) (Hymenoptera: Encyrtidae) for augmentative release against black scale, Saissetia oleae (Olivier) (Homoptera: Coccidae). Masters thesis, University of California, Riverside California. 140pp. Webber, H.J., Reuther, W., Lawton, H.W History and Development of the Citrus Industry, In: The Citrus Industry, Vol. 1.Univ. Calif. Press, Berkeley CA. Yu, D.S., Luck, R.F., Murdoch, W.W Competition, resource partitioning and coexistence of an endoparasitoid Encarsia perniciosi (Tower) and ectoparasitoid Aphytis melinus DeBach (Hymenoptera: Aphelinidae) of the California red scale (Homoptera: Diaspididae). Ecol. Entomol. 15,

13 THE STATUS OF BIOLOGICAL CONTROL IN SAN JOAQUIN VALLEY CITRUS Elizabeth E. Grafton-Cardwel1 l and Neil V. O Connell 2 1 Department of Entomology, University of California, Riverside, CA University of California Cooperative Extension, Tulare, CA INTRODUCTION In the early years of California citrus production, the majority of citrus was grown in the southern region of the state. Early successes with releases of vedalia beetle Rodolia cardinalis (Mulsant) (Coleoptera: Coccinellidae) to control cottony cushion scale Icerya purchasi Maskell (Homoptera: Margarodidae) (Caltagirone and Doutt, 1989) spawned both inoculative and augmentative releases of natural enemies for mites, whiteflies, armored scales, soft scales and mealybugs in that region (Clausen, 1978). In addition, researchers developed economic thresholds of damage and monitoring methods for a number of pests including citrus thrips Scirtothrips citri (Moulton) (Thysanoptera: Thripidae) and citrus red mite Panonychus citri (McGregor) (Acari: Tetranychidae) (Grout et al., 1986: Zalom et al., 1986; Rhodes and Morse, 1989; Hare et al., 1992). These advances allowed growers to rely heavily on natural enemies and today, the majority of growers in southern California have adopted biologicallybased integrated pest management (IPM) practices. In recent years, urbanization of southern California has shifted citrus acreage to the San Joaquin Valley (SJV), so that now more than 70% of the acreage is located in that region. SJV citrus growers have been much slower to adopt biological control methods because natural enemies have traditionally not prospered as well in that region of California. In the SJV, winters are much colder and summers much hotter than southern California, which limits natural enemy effectiveness. For example, early instars of California red scale Aonidiella aurantii (Maskell) (Homoptera: Diaspididae) experience severe mortality during the winter. In the spring, the pest population consists primarily of males and late stage females that produce crawlers in early May. The parasitoid Aphytis melinus DeBach (Hymenoptera: Aphelinidae) prefers to parasitize 3 rd instar nongravid female scales and, in the SJV region, there are periods of time in the spring and early summer when that stage is unavailable and the parasitoid population growth lags (Yu and Luck, 1988). In southern California, all stages of A. aurantii are available year-round and parasitism progresses more easily. Because of the greater difficulty in achieving biologically-based IPM, SJV citrus growers have, in the past, taken a more conservative approach to pest management. These growers relied on organophosphate and carbamate insecticides well into the 1980s because they were cheap and effective. Since these classes of insecticides were toxic to natural enemies (Morse and Bellows, 1986; Bellows and Morse, 1988), SJV growers did not make use of natural enemies to the same degree as in Southern California. In the mid 1980 s, a group of UC researchers, farm advisors and pest control advisors from both southern California and the SJV, with funding provided by the Citrus Research Board, California Energy Commission, and USDA Office of International Cooperation and Development, tested a biologically-based citrus IPM program in Tulare County using methodologies and concepts originally developed in southern California. The program emphasized using intensive pest monitoring methods to reduce the frequency of insecticide treatments and selective insecticides to allow natural and augmented populations of natural enemies to survive (Haney et al., 1992; Luck et al., 1992; 1997). For citrus thrips, the program utilized the botanical sabadilla (Veratran D); for citrus cutworm Egira curialis (Grote) (Lepidoptera: Noctuiidae) and fruittree leafroller Archips argyrospila (Walker) (Lepidoptera: Tortricidae) growers used various formulations of Bacillus thuringiensis (Bt); for citrus red mite, growers used narrow range oil; for forktailed bush katydid, Scuddaria furcata Brunner von Wattenwyl (Orthoptera: Tettigoniidae) and citricola scale Coccus pseudomagnoliarum (Kuwana) (Homoptera: Coccidae), growers used low rates of the organophosphate chlorpyrifos (Lorsban); and they managed California red scale through augmentative releases of 100,000 insectary-reared A. melinus parasitoids per acre per year. Parasitoids were released every two weeks beginning mid February and ending mid November each year for 20 releases of 5,000 wasps per acre. Low rates of chlorpyrifos were used to reduce California red scale levels prior to initiating the A. melinus releases. Low rates of chlorpyrifos were found to be compatible with the IPM program because after many years of organophosphate treatments, a number of key natural enemies had developed moderate levels of resistance and could tolerate occasional use (Rosenheim and Hoy, 1986; Grafton-Cardwell and Ouyang, 1993). The biologically-based program was demonstrated to produce similar fruit quality and economic returns compared with the conventional broadspectrum pesticide-based program (Haney et al., 1992; 1994). These practices were incorporated into the UC IPM Citrus Pest Management Guidelines and the sampling and treatment recommendations were utilized by many growers. While augmentative A. melinus releases were important for control of California red scale, use of selective pesticides for pests with ineffective biological control helped to preserve naturally occurring predators and parasites 8

14 important for suppressing a number of other pests. For example, during the early season, soft pesticides for citrus thrips and low rates of chlorpyrifos for katydids allowed the predatory mite Euseius tularensis (Congdon) (Acari: Phytoseiidae) to survive and assist with citrus red mite and citrus thrips control, vedalia beetle to survive to control cottony cushion scale, and various parasitoids to survive to control pest Lepidoptera. Use of oils and low rates of chlorpyrifos for scales during the latter part of the season allowed the parasitoid Comperiella bifasciata Howard (Hymenoptera: Encyrtidae) as well as lacewings and coccinellid beetles to assist with control of California red scale. Supported with funding from the Smith-Lever Program ( ) and later the Cal DPR Pest Management Alliance and Citrus Research Board funds ( ), citrus pests were sampled in a mixture of commercial citrus orchards using conventional and A. melinus-release treatments in Tulare County to demonstrate that the two programs produced similar low levels of insect damaged fruit in the SJV (Grafton-Cardwell et al., 1995; Grafton-Cardwell 2002). Yearly workshops were held to teach pest control advisors how to recognize the stages of California red scale and their parasitoids, and how to determine if biological control was successful (Forster et al., 1995). Training video tapes describing the biology and monitoring methods for citrus red mites, citrus thrips, California red scale, and Lepidoptera were produced. Monthly field days were conducted to demonstrate the biology of citrus pests and sampling techniques using a mobile laboratory and funding from the Western Regional IPM program ( ). In addition, a number of roundtable discussions were jointly sponsored by the University of California Cooperative Extension and the Association of Applied IPM Ecologists. In these discussions, pest control advisors shared information about pest pressures, monitoring methods, control tactics, and the level of success of biological control they had achieved. Data on pest densities, natural enemy densities, degree-days, and the consequences of various pest management strategies were posted on a citrus entomology web site at the Kearney Agricultural Center ( This educational activity helped to increase grower adoption of biologically-based IPM methods. At the peak of its acceptance, the biologically-based program including A. melinus releases, was adopted by approximately 25% of SJV growers. The reasons that full adoption was not higher were: 1) the program required intensive sampling procedures to determine when economic thresholds had been reached, 2) some of the pesticide treatments, especially sabadilla for citrus thrips, were less effective than broad spectrum pesticides, and 3) some of the pests, notably citricola scale, did not have effective biological control, requiring broad spectrum pesticides that disrupted the A. melinus release program. PESTICIDE RESISTANCE SERVES AS AN IMPETUS FOR CHANGE While education was very important for grower adoption of biological control methods, the most significant stimulus for adoption of the SJV biologically-based citrus IPM program was the development of pesticide resistance by two key pest species, citrus thrips and California red scale. Citrus thrips developed resistance to the organophosphate dimethoate in 1980, the carbamate formetanate in 1986, and the pyrethroid cyfluthrin in 1996 (Morse and Brawner, 1986; Immaraju et al., 1989; Khan and Morse, 1998). Of greater impact, however, was the development of resistance to organophosphate and carbamate insecticides in California red scale in the SJV in the 1990s (Grafton-Cardwell and Vehrs, 1995; Grafton-Cardwell et al., 2001). The lack of residuality of the insecticides forced growers to treat nearly every generation of scale (4 generations per year). As resistance increased, growers escalated their use of organophosphate and carbamate insecticide treatments for scales from every other year to 2-4 applications per year. Initially, no new chemical options were available to growers with insecticide-resistant California red scale, and because multiple applications of organophosphates and carbamates were so costly (ca. $160/acre per treatment), grower adoption of the biologically-based citrus IPM program accelerated in the early 1990 s and reached a peak in 1997 as resistance in California red scale peaked. Growers looking for alternatives to organophosphate and carbamate insecticides utilized oil treatments to reduce red scale populations followed by A. melinus releases. A high-pressure post-harvest washer technology was brought from South Africa to SJV packing-houses to remove California red scale from fruit (Walker et al., 1996). This technology helped to raise grower tolerance for California red scale infestation of fruit. REDUCED RISK AND ORGANOPHOSPHATE-REPLACEMENT INSECTICIDES INTRODUCED During the 1990s and early 2000s a number of new insecticides were registered for citrus and introduced into the SJV IPM program to replace what had been an organophosphate and carbamate-based program for more than 40 years. For citrus thrips, the fermentation product abamectin (Agri-Mek), the pyrethroids cyfluthrin (Baythroid) and fenpropathrin (Danitol), and the reduced-risk insecticide spinosad (Success) replaced formetanate and dimethoate. Replacement insecticides for California red scale arrived in the form of two reduced-risk insect growth regulators (IGRs), buprofezin (Applaud) and pyriproxyfen (Esteem). Finally, in 2001 and 2002 the neonicotinoids imidacloprid (Admire and Provado) and acetamiprid (Assail) received registration as reduced-risk and/or organophosphate replacements. The neonicotinoids are not very effective against key pests such as citrus 9

15 thrips and California red scale, however, they are moderately effective against citricola scale and the newly introduced glassy-winged sharpshooter, Homalodisca coagulata (Say) (Hemiptera: Cicadellidae). Table 1 shows the number of insecticides applied to Tulare County citrus orchards during before the new insecticides had been introduced. On average, pesticide treatments per orchard were applied and of those treatments were applied as tank mixes. The most common tank mix during this time period was a combination of organophosphate and carbamate insecticides for citrus thrips in an attempt to combat increasing levels of resistance of citrus thrips to these insecticides. Key pests during that time period were citrus thrips and California red scale. The primary treatments for thrips and katydids (Table 2) were sabadilla for the biologicallybased program and organophosphate and carbamate insecticides for the conventional program. The primary treatments for scales were oils for the biologically-based program and organophosphate and carbamate insecticides for the conventional program. During , after the introduction of the new insecticides, the number of treatments per orchard ranged from and treatments were applied as tank mixes. Key pests during that time period were citrus thrips, katydids, citricola scale, and California red scale. The most common tank mix during was a combination of spinosad for citrus thrips with either an organophosphate or a pyrethroid for katydids. The primary treatments for scales were organophosphates for citricola scale and IGRs for California red scale. Thus, organophosphate insecticides were retained for katydids and citricola scale. Carbamate use was eliminated by the new insecticides. Sabadilla use was eliminated due to the greater efficacy of spinosad for citrus thrips. Because of the high efficacy of some of the new insecticides, conventional growers rapidly adopted them, especially spinosad for citrus thrips and pyriproxyfen for California red scale. Growers practicing biologically-based IPM adopted these same insecticides because of their selectivity favoring natural enemies as well as increased efficacy. Thus, the differences in insecticide choices between conventional and biologically-based growers have lessened. Organophosphate and carbamate use declined by more than 70%, in the SJV, between 1997 and 2000 because new insecticides became available to control OP and carbamate-resistant citrus thrips and California red scale (Grafton-Cardwell, 2000b; CDPR ). This reduction in OP and carbamate use was hailed by Cal EPA as successful replacement of organophosphate and carbamate insecticides with safer, reduced risk insecticides. However, while the new insecticide classes are much better for human health, they have created some interesting dilemmas for the citrus IPM program. On the positive side, the greater selectivity of spinosad and pyriproxyfen compared to organophosphate and carbamate insecticides has allowed greater survival of parasitoids and most groups of predators in both the conventional and the biologically-based orchards than ever before. This reduces the need for insecticides for pests with effective biological control such as California red scale, citrus red mites and Lepidopteran pests. A good example of this is that in the early 1990s, fruittree leafroller was a common pest in citrus orchards and in the 2000s it has been rarely observed. The problem with greater selectivity of the new insecticides is that several pests that have inadequate biological control in the SJV and that were easily controlled by organophosphate and carbamate sprays for citrus thrips and California red scale, are now released from control because the new insecticides are not effective for these pests. Both katydids and citricola scale have become primary pests since the valley-wide reduction in organophosphate and carbamate insecticide use. Citricola scale is virtually nonexistent in southern California because the milder climate allows more overlap of stages, there is a higher incidence of alternative hosts such as black scale and brown soft scale, and possibly because southern California has a different parasitoid complex attacking the pest. In the SJV, citricola scale has become common and parasitoids do not maintain populations below the economic threshold of 0.5 nymphs per leaf. Katydids and citricola scale populations are now frequently requiring additional broad spectrum insecticide treatments above and beyond those applied for citrus thrips and red scale, as reflected in the data. This problem was experienced by the biologically-based IPM orchards in the early 1990s as they halted organophosphate use. Now it is being experienced by growers in all types of pest management programs as they rely heavily on spinosad for citrus thrips and pyriproxyfen for California red scale. In spite of these problems, on average, the number of applications of insecticides used in SJV citrus has dropped to less than three per orchard with the advent of the new insecticide groups (Table 1). The number of treatments per orchard and sprayer costs are kept low by tank-mixing the thrips/katydid treatments and by treating in alternate years with pyriproxyfen for California red scale and chlorpyrifos for citricola scale. One natural enemy, the vedalia beetle R. cardinalis, was severely negatively affected by the shift to the new insecticide classes. This predatory beetle has successfully controlled cottony cushion scale since its establishment in the late 1800s and is one of the most famous classical biological control stories (Caltagirone and Doutt, 1989). Cottony cushion scale was disrupted by carbamates and organophosphates when they were first introduced (Ebling, 1959), but has developed high levels of resistance to these insecticide classes. Unhappily, both field trials and laboratory tests (Grafton-Cardwell and Gu, 2003) have shown that the vedalia beetle has an extreme 10

16 sensitivity to IGR (buprofezin, pyriproxyfen), neonicotinoid (acetamiprid, imidacloprid), and pyrethroid (cyfluthrin, fenpropathrin) insecticides introduced to SJV citrus in recent years. Many of these insecticides, except pyrethroids, cause little or no mortality of the cottony cushion scale. The broad spectrum neonicotinoids and pyrethroids kill beetles and larvae directly and the IGRs prevent the pupae from completing development and in the case of Esteem prevents the eggs from hatching. This effect can last for many months, allowing cottony cushion scale populations to expand unchecked. Cottony cushion scale populations reached outbreak proportions in the SJV following the introduction of pyriproxyfen (Grafton-Cardwell, 1999; 2000a). Hattingh (1995) saw a similar problem with insect growth regulators and coccinellid beetle predators in South Africa. While pyriproxyfen was the most obvious culprit because of heavy initial use (50,000 acres treated in 1998), other insecticides have also caused problems. Cottony cushion scale outbreaks have subsided since the amount of pyriproxyfen-treated acreage has declined and growers have learned to apply treatments after vedalia beetles have had time to eliminate the cottony cushion scale in the spring. However, as citrus growers tank-mix pyrethroids to obtain katydid control they are likely to disturb the springtime effectiveness of vedalia beetles. Thus, insect growth regulators, the neonicotinoids and pyrethroids are not fully compatible with citrus IPM. CURRENT IMPEDIMENTS TO ADOPTION OF BIOLOGICALLY-BASED CITRUS IPM IN THE SJV Currently, there are three impediments to maintaining and expanding reliance on biologically-based IPM in SJV citrus. First, both katydids and citricola scale are lacking effective biological control agents. Fig. 1 shows that the number of broad spectrum pyrethroid and organophosphate treatments reached a low in 2000, but use is escalating as of 2004 in response to increasing katydids (CDPR ). Fig. 2 shows that the number of organophosphate treatments reached a low in 2000, but is increasing in response to citricola scale (CDPR ). Katydids can be controlled with selective insecticides such as cryolite (Kryocide) and diflubenzuron (Dimilin). However, these insecticides are slow acting and so intensive sampling and early treatment (prior to petal fall) is critical for their success. Citricola scale is currently the most serious stumbling block to adoption of biologically-based IPM in the SJV. A number of parasitoids have been collected from Asia and released in California (Kennett et al., 1995), and these parasitoids have effectively controlled citricola scale in southern California. However, they have not controlled the pest in the SJV region. In the SJV, the extremes of summer heat and winter cold synchronize citricola scale stages so that there are long periods of time when the scale stages needed for parasitism by Metaphycus and Coccophagus parasitoids (2 nd instars) are not available (Bernal et al., 2001). The lack of alternative hosts such as brown soft scale and black scale also poses a problem in the SJV. Further, there are no effective, selective insecticides available for citricola scale. The majority of growers use chlorpyrifos, and to a lesser extent acetamiprid and imidacloprid for citricola scale control. Recent complaints about chlorpyrifos efficacy have stimulated research, and we have preliminary evidence that citricola scale may be developing resistance to chlorpyrifos. Secondly, even if biological and/or selective chemical control of citricola scale is achieved, biologicallybased IPM will continue to be challenged with each introduction of a new pest species. When exotic pests enter a region, they often arrive without a full compliment of natural enemies from their native range. Thus, chemical control is often needed to reduce damage below economic thresholds until the full natural enemy complex is introduced and provides control. If the pest is a quarantine pest, eradication is required and nearly always demands broad spectrum pesticides, because biological control and soft pesticides can not eradicate incipient pest populations. An example of an exotic pest that recently entered California is the glassy-winged sharpshooter (GWSS), Homalodisca coagulata (Say). GWSS lives on citrus (as well as many other hosts) and vectors various strains of the bacterium Xylella fastidiosa that cause Pierce s Disease (PD) in grapes. There is currently no cure for PD, which causes the death of susceptible varieties of grape within 1-3 years. Because this pest is so destructive to the grape industry and because citrus is a preferred oviposition host (Park et al., 2006), citrus growers are required to reduce GWSS in citrus to minimize the movement of Xylella into nearby grapes. A difficulty for the biologicallybased citrus IPM program, is that GWSS is best controlled by broad spectrum pyrethroids and the neonicotinoid insecticides (Grafton-Cardwell et al., 2003), potentially causing secondary pest outbreaks of California red scale, mites, and cottony cushion scale. There are no fully IPM compatible insecticides for glassy-winged sharpshooter control. Biological control agents are released for GWSS in urban areas, however, insecticides are used in citrus to gain more rapid reduction of the pest. The problem of exotic pest introductions appears to be on the rise because of increased movement of humans and plant material within and between states and countries. Finally, sugar-feeding ants, especially Argentine ants Linepithema humile (Mayr) and native gray ants Formica aerata (Francouer) (Hymenoptera: Formicidae), protect homopteran pests from parasites and predators and reduce the success of biological control programs in the SJV. In years past, broad spectrum pesticides applied for thrips and scales suppressed ant populations. The arrival of the red imported fire ant Solenopsis invicta Buren 11

17 spawned development of corn-cob grit baits treated with various toxicants that have been effective for fire ant control in agricultural crops. However, these types of baits can not be utilized by Argentine and native gray ants, which are better adapted to utilize liquid sugar. Research is underway to determine the distribution of stations and types of toxicants mixed in liquid-sugar solutions that could be used in baiting stations (Tollerup et al., 2004). Worker ants feeding at the station need to take in a low enough dosage of the toxicant that the ant is not killed immediately, but brings the toxicant back into the nest and feeds it to the immature stages. This type of ant control is perceived as a small market by the chemical industry and so it is only recently that several companies have taken an interest in registering toxicants in sugar solution for agricultural crops with Cal EPA. Registration of organic and non-organic toxicants in bait stations will greatly improve the success of biological control in the SJV. In general, the majority of SJV citrus growers are practicing IPM in the sense that they sample for pests, treat only when necessary, and whether they know it or not, they are using fairly selective pesticides that allow natural enemies to survive and assist with control. SJV growers can rely on natural enemies for citrus red mite, lepidopteran pests, and California red scale. Citrus thrips and katydids can be managed with a combination of natural enemies and selective insecticides. Citricola scale is currently the most intractable pest, lacking effective natural enemies and requiring the use of broad spectrum pesticides that disrupt biological control of the other pests. If the citricola scale problem could be solved, then pesticides would be reduced, lessening the risk of secondary outbreaks of secondary pests and the development of pesticide resistance in key pests. ACKNOWLEDGEMENTS We would like to acknowledge Ashley Derr and Yvonne Rasmussen for collection of the data and Neil and Lisa Munoz and Garrett Lehman for collection of the data. REFERENCES Bellows T.S. Jr., Morse, J.J Residual toxicity following dilute or low-volume applications of insecticides used for control of California red scale (Homoptera: Diaspididae) to four beneficial species in a citrus agroecosystem. J. Econ. Entomol. 81, Bernal J.S., Morse J.G., Luck R.F., Drury M.S Seasonal and scale size relationships between citricola scale (Homoptera: Coccidae) and its parasitoid complex (Hymenoptera: Chalcidoidea) on San Joaquin Valley citrus. Biol. Control 20, Caltagirone L.E., Doutt, R. L The history of the vedalia beetle importation to California and its impact on the development of biological control. Ann. Rev. Entomol. 34, California Department of Pesticide Regulation (CDPR) Annual pesticide use data. Environmental Monitoring and Pest Management Branch. Sacramento, CA. ( Clausen C.P Biological control of citrus insects. In: The Citrus Industry Vol. IV, Crop protection. University of California Division of Agricultural Sciences, pp Ebling, W Subtropical Fruit Pests. University of California, Division of Agricultural Sciences,. pg 175. Forster L.D., Luck R.F., Grafton-Cardwell E.E Life stages of California red scale and its parasitoids. University of California, Division of Agriculture and Natural Resources Pub , Oakland, CA. Grafton-Cardwell E.E Pesticide disruption of vedalia beetle results in cottony cushion scale outbreaks. KAC Plant Protection Quarterly 9, Grafton-Cardwell E.E. 2000a. Citrus: Integrating Biological Control and Insecticide Treatments for Cottony Cushion Scale and Other Scale Pests. In: Proc. California Conference on Biological Control II, July 11-12, 2000, Riverside, CA. pp Grafton-Cardwell E.E. 2000b. Citrus IPM in California: regional differences and their effects on arthropod management in the millennium. In: Proceedings of the International Society of Citriculture, 9 th International Citrus Congress, Orlando Florida. Grafton-Cardwell E.E Can reduced risk pesticides upset biological control of citrus pests? In Proc. California Conference on Biological Control III, Aug 15-16, 2002, Davis, CA. pp , Grafton-Cardwell E.E., Gu P Conserving vedalia beetle, Rodolia cardinalis (Mulsant) (Coleoptera: Coccinellidae), in citrus: a continuing challenge as new insecticides gain registration. J. Econ. Entomol. 96, Grafton-Cardwell E.E., Ouyang Y Toxicity of four insecticides to various populations of the predacious mite; Euseius tularensis Congdon (Acarina: Phytoseiidae) from San Joaquin Valley California citrus. J. Agric. Entomol. 10,

18 Grafton-Cardwell E.E., Reagan C.A Selective use of insecticides for control of armored scale (Homoptera: Diaspididae) in San Joaquin Valley California Citrus. J. Econ. Entomol. 88, Grafton-Cardwell E.E., Vehrs S.L.C Monitoring for organophosphate- and carbamate-resistant armored scale (Homoptera: Diaspididae) in San Joaquin Valley citrus. J. Econ. Entomol. 88, Grafton-Cardwell B., Eller A., O Connell N Integrated citrus thrips control reduces secondary pests. Calif. Agric. 49 (2), Grafton-Cardwell E., Ouyang Y., Striggow R., Vehrs, S Armored scale insecticide resistance challenges San Joaquin Valley citrus growers. Calif. Agric. 55(5), Grafton-Cardwell E.E., Reagan C.A., Ouyang Y Insecticide treatments disinfest nursery citrus of glassywinged sharpshooter. Calif. Agric. 57(4), Grout T.G., Morse J.G., O Connell N.V., Flaherty D.L., Goodell P.B., Freeman M.W., Coviello R.L Citrus thrips (Thysanoptera: Thripidae) phenology and sampling in the San Joaquin Valley California. J. Econ. Entomol. 79, Haney P.B., Morse J.G., Luck R.F., Griffiths H., Grafton-Cardwell E.E., O'Connell N.V Reducing insecticide use and energy costs in citrus pest management. UC IPM Publication 15, University of CA, Statewide IPM Project, DANR, Oakland CA, 62 pp. Haney P.B., Morse J.G., Luck R.F., Amon R Pest management in California citrus: an economic analysis. Proc. Intern. Soc. Citriculture Vol. III, Hare J.D., Pehrson J.E., Clemens T., Menge J.A., Coggins Jr. C.W., Embleton T.W., Meyer J.L Effect of citrus red mite (Acari: Tetranychidae) and cultural practices on total yield, fruit size, and crop value of navel orange: years 3 and 4. J. Econ. Entomol. 85, Hattingh V.T.B Effects of field-weathered residues of insect growth regulators on some Coccinellidae (Coleoptera) of economic importance as biocontrol agents. Bull. Entomol. Res. 85, Immaraju J.A., Morse J.G., Kersten, D.J Citrus thrips (Thysanoptera: Thripidae) pesticide resistance in the Coachella and San Joaquin valleys of California. J. Econ. Entomol. 82, Kennett C.E., Hagen K.S., Daane K.M Citricola scale. In: Biological Control in the Western United States. University of California Division of Agriculture and Natural Resources. pp Khan I., Morse J.G Citrus thrips (Thysanoptera: Thripidae) resistance monitoring in California. J. Econ. Entomol. 91, Luck R.F., Morse J.G., Haney P.B., Griffiths H.J., Barcinas J.M., Roberts T.J., Grafton-Cardwell E.E., O'Connell N.V Citrus IPM - It Works! Calif. Grow 16(4), Luck R.F., Forster L.D., Morse J.G An ecologically based IPM program for citrus in California s San Joaquin Valley using augmentative biological control. Proc. Intern. Soc. Citriculture, 1996, Vol. 1, Morse J.G., Bellows T.S Toxicity of major citrus pesticides to Aphytis melinus (Hymenoptera: Aphelinidae) and Cryptolaemus montrouzieri (Coleoptera: Coccinellidae). J. Econ. Entomol. 79, Morse J.G., Brawner, O.L Toxicity of pesticides to Scirtothrips citri (Thysanoptera: Thripidae) and implications to resistance management. J. Econ. Entomol. 79, Park Y-L., Perring T.M., Farrar C.A., Gispert C Spatial and temporal distributions of two sympatric Homalodisca spp. (Hemiptera : Cicadellidae): Implications for areawide pest management. Agriculture Ecosystems & Environment 113, Rhodes A.A., Morse J. G Scirtothrips citri sampling and damage prediction on California navel oranges. Agric. Ecosystems and Environ. 26, Rosenheim J.A., Hoy M.A., Intraspecific variation in levels of pesticide resistance in field populations of a parasitoid; Aphytis melinus (Hymenoptera: Aphelinidae): The role of past selection pressures. J. Econ. Entomol. 79, Tollerup K.D., Rust M.K., Dorschner K.W., Phillips P.A., Klotz J.H Low-toxicity baits control ants in citrus orchards and grape vineyards. Calif. Agric. 58, Walker G.P., Morse J.G., Arpaia M.L Evaluation of a high-pressure washer for postharvest removal of California red scale (Homoptera: Diaspididae) from citrus fruit. J. Econ. Entomol. 89, Yu D.S., Luck R.F Temperature-dependent size and development of California red scale (Homoptera: Diaspididae) and its effect on host availability for the ectoparasitoid Aphytis melinus DeBach (Hymenoptera: Aphelinidae). Environ. Entomol. 17, Zalom F.G.; Wilson L.T.; Kennett C.E, O Connell N.V., Flaherty D.L., Morse J.G Presence-absence sampling of citrus red mite Panonychus citri. Calif. Agric. 40 (3-4),

19 Table 1. Mean number of pesticides per orchard applied to 10 orchards during and a second set of 10 orchards during in Tulare County, CA. Target Pest Citrus red mite Lepidoptera Citrus thrips & katydid Scales Avg. # insecticides per orchard No. tank mix combinations Table 2. Mean number of insecticide treatments per orchard by chemical class applied to 10 orchards during and a second set of 10 orchards during in Tulare County, CA. Target Pest Pesticide class Citrus thrips/ katydids Scales Botanical OP Carbamate Pyrethroid Abamectin Spinosad Oil OP Carbamate IGR

20 Fig. 1. Acres treated with various insecticides groups (organophosphates, carbamates, abamectin, sabadilla and spinosad) for control of citrus thrips and katydids during in the San Joaquin Valley, CA. 300, , , , ,000 50, Acres Treated OP/Carb pyrethroid abamectin sabadilla spinosad Fig. 2. Acres treated with various insecticides groups (carbamates, organophosphates, pyriproxyfen, buprofezin) for control of scales during in the San Joaquin Valley, CA. 200,000 Acres Treated 150, ,000 50, carbamate OPs pyriproxyfen buprofezin 15