Interim Report Biological Control of Arthropod Pests in California Agriculture: Current Status and Future Potential Kent M. Daane 1, Nicholas J. Mills 1, Keith D. Warner 2, and Christy Getz 1, Steve C. Welter 1 1 Dept. Environmental Science, Policy and Management, University of California, Berkeley 2 Environmental Studies Institute, Santa Clara University Contents Preface ............................................................................................................................................ 2 The Missing Metrics of Classical Arthropod Biological Control in the USA .......................... 4 Commodifying Insects? Challenges to the Commercialization of Augmentative Biocontrol in Agriculture ................................................................................ 5 A Socio-Economic Analysis of the North American Insectary Industry and Implications for Augmentative Biological Control ............................................ 7 Biological Control of Key Pests in Cotton .................................................................................. 8 Biological Control of Key Pests in Lettuce ............................................................................... 34 Biological Control of Key Pests in Grapes ................................................................................ 44 Biological Control of Key Pests in Apples and Pears .............................................................. 75 Development of Biological Controls in Stone Fruit ................................................................ 96 Biological Control of Insects and Mites in Almonds ............................................................. 114 Biological Control of Arthropod Pests in California Agriculture Preface California agriculture is a $32 billion industry and one of the state’s leading sources of revenue and employment (2006, http://www.cdfa.ca.gov/files/pdf/card/AgResDirEntire06.pdf). Arthropod pests, both invasive and indigenous, have the potential to cause severe damage to California agricultural industry. Insecticides are commonly used to protect California’s agricultural industry from arthropod pests. However, public concerns for contamination of food, water, the environment, and impacts on human health have brought insecticide use under increased scrutiny. Insecticides are among non-point source discharges that will be increasingly regulated and are currently under pressure from the EPA and State and Regional Water Quality Control Boards (under Cal EPA) as a result of implementation of the Food Quality Protection Act (FQPA) and the Clean Water Act (CWA). Thus, alternative control methods to the traditional insecticides must be developed and tested in the near future to maintain an economically viable agricultural industry in California. Biological control offers a proven management alternative for many arthropod pest problems. Biological control is based upon a fundamental knowledge of the interactions of living organisms, makes use of living natural enemies for the control of pests, and provides a sound ecological basis for pest management in many of California’s crop systems. Successful biological control programs can enhance farm and ecosystem sustainability, reduce fuel inputs, and reduce human risk and non-target organism exposure to toxic pesticides. If biological control can offer clear economic and sustainable control solutions to many arthropod pest problems, then why has there not been greater adoption of potentially successful practices and more research funding to develop new programs? The following interim report covers two broad areas. First, we attempt to identify organizational and legislative barriers to adoption of biological control with a view to targeting critical needs for research and implementation in California agriculture. Second, we sought to summarize the history and current status of biological control in selected California crops, as well as future constraints and opportunities for these crops. 1) To identify key barriers and opportunities for greater implementation of biological control in pest management in California Biological, economic, institutional and social factors can be considered as barriers to natural enemy importation. Our ability to select the most effective natural enemy from the region of origin of an invasive pest will be considered, together with current and expected future changes in the federal and state permitting procedures for exotic natural enemies. We will also consider the consequences of FQPA and its impact on the registration of selective reduced risk insecticides. The changes over the last 50 years in California’s research programs and personnel in biological control (UC, USDA, CDFA) will be documented, changes in levels of funding support for foreign exploration and quarantine operations will be analyzed from records (UC campuses, commodity funding), and adjustments to the priorities of the different agencies involved (UC, CSU, USDA, CDFA) will be determined. The recent change in social attitudes toward the environment, exotic species and non-target impacts of imported biological control agents will be considered, as well. Barriers for successful application of mass reared natural enemies include the economies of scale, lack of a “patentable” product or methodology and thus economic sustainability, quality control of the natural enemies produced, linkages and partnerships required in moving from production to implementation, and the greater knowledge base required of all participants. The importance of these perceived barriers was 2 Biological Control of Arthropod Pests in California Agriculture evaluated by gathering data from in-depth interviews with end users, particularly insectary producers (Association of Natural Biocontrol Producers), commodity research directors, the Organic Farming Research Foundation, and PCAs (particularly those affiliated with the Association of Applied IPM Ecologists). In addition, we analyzed changes in funding support (federal, state, and commodity boards grants) and research efforts (primarily personnel at the UC, CSU, USDA and CDFA) over the last 50 years for augmentative biological control. One important variable that defines the backdrop for all pest management is the choice and frequency of insecticide applications for key pests. Insecticide programs have varied widely over time, and changes coming as a consequence of the implementation of FQPA and CWA and their impacts on insecticide development, have the potential to increase the opportunities for biological control. Previous assessments that examined the economic impact of the elimination of OP insecticides on California agriculture [Metcalfe et al. 2002. “The economic impact of organophosphates in California agriculture.” California Department of Food and Agriculture Report, http://www.cdfa.ca.gov/publications.html ] served as the platform for further analysis. Using data from the literature and from the Department of Pesticide Regulation’s pesticide use database on historical trends in pesticide use and selectivity of pesticides, the changing pattern of past, present and future opportunities for conservation of natural enemies in production agriculture is being documented. 2) Document historical benefits in key commodities. The academic and popular literature has been reviewed to document the history of biological control attempts and successes in key agricultural crops in California. The review considered natural enemy importation, periodic releases of mass reared natural enemies and management practices that have been adopted to enhance the activity of natural enemies in these crops. Crops selected for review include annual row crops (cotton and lettuce) and perennial crops (almond, grape, pome fruit, and stone fruit). Information was gathered from the scientific literature, commodity reports, the University of California Integrated Pest Management manuals and project database, the USDA ROBO database of biological control importations, and from the quarantine facilities of UC Berkeley, Davis and Riverside. This will provide a chronologically-organized list of biological control programs over the last 100 years targeting major arthropod pests attacking these key commodities in California. Our future plans are to use the crop summaries to design a set of categorical descriptions including crop characteristics (value, perennial versus annual, damage tolerance), operational practices (insecticide use, timing, disturbance levels), pest characteristics (taxa, biological traits, phenology), and natural enemy characteristics (taxa, biological traits, past successes). These characteristics will be used as a basis for developing an overall rating of the future potential for biological control. The result will be a description of insect pests and commodities that have “high potential” as targets for biological control. For example, an aphid pest of lettuce that has a low economic injury threshold may be a poor target, while a scale pest in almonds may have greater potential. These ratings can then be used to identify funding priorities or allocation of resources within agencies to crops or target pests which either have the greatest opportunities for success or present the greatest challenges. 3 The Missing Metrics of Classical Arthropod Biological Control in the USA The Missing Metrics of Classical Arthropod Biological Control in the USA Keith Warner 1, Christy Getz 2, Stephen Maurano 1, and Kathleen Powers1 1 Environmental Studies Institute, Santa Clara University 2 Dept. Environmental Science, Policy and management, University of California Berkeley Abstract submitted to Environmental Entomology Increasing concerns about potential nontarget effects of classical biological control have prompted efforts to evaluate relative risks, costs and benefits of proposed introductions. This study reviews publicly available data collected to assess classical biological control projects targeting arthropods in the USA. After reviewing recent retrospective analyses of risks, it then examines the use of metrics used to evaluate classical biological control of arthropods. Available data are then presented on biocontrol introductions in 3 states since 1962. Existing record keeping systems were established prior to widespread concern about nontarget effects of introduced control agents, and offer incomplete and inconsistent data for evaluating risks, costs and benefits. No economic analysis of a classical biological control project targeting agricultural arthropod pests has been published in the USA within the past 30 years. Hawaii, California and Florida have been the states hosting the most projects, but rates of introductions in all 3 states have declined over the past 15 years. We discuss the implications of these data and its limitations, and propose strategies for making possible more complete cost/benefit/risk analyses. 4 Commodifying Insects? Challenges to the Commercialization of Augmentative Biocontrol in Agriculture Commodifying Insects? Challenges to the Commercialization of Augmentative Biocontrol in Agriculture Christy Getz 1 and Keith Douglass Warner 2 1 Dept. Environmental Science, Policy and Management, University of California, Berkeley 2 Environmental Studies Institute, Santa Clara University Abstract Augmentative biological control has been advanced by scientists as an alternative to agrochemical pesticides for many years (suggested by our respondents, and those interviewed by Ridgway and Inscoe 1998; Ridgway, King, and Carillo 1977; Justum 1988; Obrycki, Lewis, and Orr 1997). Parella, Heinz, and Nunney (1992) went so far as to title an article “biological control through augmentative releases of natural enemies: a strategy whose time has come.” The cancellation of pesticide registration, rising threat of pesticide resistance, public distaste for pesticides, and expansion of organic agriculture have been proposed as factors favoring augmentative biological control (Ridgway and Inscoe 1998), especially in annual cropping systems (Obrycki, Lewis, and Orr 1997). Some have cited the increasing number of commercial distributors as evidence of growing supply and distribution (Cranshaw, Sclar, and Cooper 1996), and van Lenteren (2003) lists 125 species available worldwide. Economic analyses have determined that the benefit to cost ratio for augmentative biological control can be as high as 3:1 in outdoor settings (Reichelderfer 1981) and 31:1 in a greenhouse (Hussey and Scopes 1985). Our research suggests, however, that augmentative biological control has not, in general, fulfilled its potential – long espoused by biocontrol scientists -- in American production agriculture. Why is this? In this paper, we conduct the first systematic commodity systems analysis of the stagnating North American commercial insectary industry. This analysis serves as a starting point for understanding biocontrol’s unfulfilled potential in production agriculture as it illuminates factors shaping the behavior of the individuals and institutions engaged in commercial natural enemy production, release, and distribution. In doing so, it sheds light on barriers and opportunities to greater economic use of commercial natural enemies as an alternative to hazardous pesticides. Specifically, following on Friedland’s (2001) methodological blueprint for commodity systems analysis, we explore the dynamic and synergistic interplay among the nodes of the natural enemy commodity chain, focusing on production, marketing and distribution, science and knowledge and consumption. We situate the entire commodity chain within the current political economic context of agriculture in the United States today. This analysis allows us to address four fundamental research questions: 1. What are the biological barriers to successful natural enemy production, rearing and distribution and how have they affected the evolution of the commercial insectary industry in North America? 2. How have economic, social, and political factors shaped the contemporary commercial insectary industry in North America? 3. Where, along the natural enemy commodity chain, do we find the key barriers to augmentative biological control achieving its oft-proclaimed potential? 4. What kind of opportunities exist for public policy to assist the industry in this regard? 5 Commodifying Insects? Challenges to the Commercialization of Augmentative Biocontrol in Agriculture In answering these questions, we demonstrate the challenges to the commodification of biocontrol, which some have described as “more of an art than a science” and as “unruly and unpredictable” given its basis in nature. Indeed, the organizational and operational processes within the natural enemy commodity chain are constrained by biological forces (Bunker 1989), and as such, natural enemy production serves as an ironic counter-movement to capital’s tendency to replace and substitute natural processes and to “squeeze biological constraints out of the production process” (Morgan et al 2006). We focus on empirical examples of challenges to Ridgway’s (1977) three proposed biological characteristics for effective augmentation: an ability to rear predictable quantities of insects of known quality; an ability to store, transport, and release the natural enemy in such a manner that it can compete at the release site; and an understanding of the ecological conditions determining the relationship between the enemy and the pest. More than just being a biological activity, however, the commercial production and release of natural enemies is simultaneously an economic, engineering and social activity, and as such, reflects scientific knowledge, technological know-how, market forces, and personal values. Whereas science and technology constitute one side of the insectary “coin,” economic profit constitutes the other. And both perspectives are essential to understanding the functioning and status of this industry. In this paper, we demonstrate that commercial augmentative biological control works when its economic (production and marketing) and biological and engineering (production, handling, shipping and performance of the agent) factors are aligned so as to be simultaneously successful. We outline the major factors that must be coordinated for successful commercial augmentative biological control, and we describe how these factors are linked though social relations in the commodity chain of natural enemy production. Additionally, we analyze the political economy of the natural enemy commodity chain. On the science and technology side, we found no evidence that any new insect species were being researched by US public agency or land-grant university scientists to be brought to market, nor were we able to identify any researchers devoting a significant portion of their time to the evaluation of new insects for commercialization of natural enemies. And we found no evidence of any institutional initiative to foster better collaboration between researchers and the insectary industry. We contextualize this glaring lack of an individual or institutional research agenda as it contrasts with significant effort and resources being poured into pesticide research, genetic engineering and other areas of pest management. Our research suggests two overarching socio-economic trends constraining the commercial application of augmentative biological control in California agriculture. First, the economic structure of agricultural pest management is generally atomistic and individualistic. Arthropod pest control decisions are most often made in reference to individual pests, as opposed to an insect complex or agroecosystem, and made by individual growers without regard to the potential benefits of agroecological landscape management. This tendency mitigates against the collaborative and coordinated scientifically-informed approaches necessary for successful augmentative biocontrol strategies, and against a market structure that would support an economically successful commercial insectary industry. Second, the orientation of scientific institutions over the last few decades has turned away from the practical, applied research necessary to support a successful commercial insectary industry. In conclusion, we suggest strategies to counter these trends and to support the development of a more vital commercial insectary industry. 6 A Socio-Economic Analysis of the North American Insectary Industry and Implications for Augmentative Biological Control A Socio-Economic Analysis of the North American Insectary Industry and Implications for Augmentative Biological Control Keith Douglass Warner 1 and Christy Getz 2 1 Environmental Studies Institute, Santa Clara University 2 Dept. Environmental Science, Policy and Management, University of California, Berkeley Abstract submitted to Biological Control This article reports the first systematic and independent socio-economic study of the commercial insectary industry in North America, drawing from 62 interviews with insectary leaders, research scientists, retail distributors, and customers. The 22 North American insectaries produce 38 natural enemy species. Commercial natural enemies constitute less than 10% of the biologically based pest control market, with an estimated gross annual value of $25-30 million at the wholesale level. Over the past decade no new insectaries have been established, several insectaries have declared bankruptcy, and only two new species have been brought into production. Producers report that the market for commercial natural enemies generally appears to be static, with declining demand for some species. Prices for at least 6 species have declined since 1994, and several insectaries report having to abandon production lines due to economic losses. Industry leaders report serious difficulties in obtaining capital for investment, researchers who will address applied scientific questions in augmentative biological control, and moving commercial natural enemies across U.S. borders. Realizing the potential of augmentative biological control as a pest management strategy in North America will require new initiatives to address these challenges. 7 Biological Control of Key Pests in Cotton Biological Control of Key Pests in Cotton Nicholas J. Mills Department of Environmental Science, Policy and Management, University of California, Berkeley, California 94720 1. Introduction The United States is one of the biggest growers and is the largest exporter of fine cotton in the world. One-third of world exports of fine cotton are grown in the San Joaquin Valley of California (Estur 2002). With an export value of $513.5 million in 2002, cotton is the number two export of California, second only to almonds (Bervejillo and Sumner 2003). In 2003, there were 700,055 acres of cotton planted in California, 671,555 acres in the San Joaquin Valley, 20,375 acres in the lower desert valleys (Coachella and Imperial) and 7,920 acres in the Sacramento Valley (Adamczyk and Burris 2004). While many arthropod species inhabit Californian cotton fields, only some are plant feeding, and economic damage can be attributed to a small subgroup of these. In 2003, pest damage destroyed 58,829 bales of cotton, which translated into a $16,942,753 loss. The same year, insecticide applications cost growers $12,454,740 (Williams 2004). The major pest species are Lygus hesperus (Het.: Miridae), Aphis gossypii (Hom.: Aphididae), Bemisia argentifolii (Hom: Aleyrodidae), Tetranychus spp. (Acar.: Tetranychidae), and a complex of Lepidoptera including Pectinophora gossypiella (Gelechiidae), Helicoverpa zea, H. virescens and Spodoptera exigua (Noctuidae). The soil inhabiting bacterium, Bacillus thuringiensis (Bt), is toxic to many lepidopteran pests. In 1990, Perlak et al. inserted genes coding for the proteins responsible for this toxicity into cotton plants. Bt cotton varieties first became available to California growers in 1996 and today, due to its effectiveness against P. gossypiella, account for 80% of the cotton grown in the Imperial Valley. However, this pest does not occur in the San Joaquin Valley, where a much smaller percentage of Bt-cotton is grown (Godfrey et al. 2005). 2. Generalist Predator Complex Another important group of arthropods inhabiting cotton is the natural enemies of insect pests. While parasitoids tend to be more specific to pest species and will be discussed in more detail in later sections, the general predator complex attacks most of the key pest species in cotton. In California, beneficial insects range from 8 to 23 insects per 50 sweep samples in organic cotton fields during the growing season (Swezey and Goldman 2001). 2.1. Big-eyed bugs: In the desert valleys the most commonly found species is Geocoris punctipes (Het: Geocoridae), while G. pallens is more common in the San Joaquin Valley (Anon. 1996). Big-eyed bugs can be present throughout the season with populations peaking during mid-summer. Both nymphs and adults are predatory, but will also feed on nectar. Alfalfa fields are an important source of big-eyed bugs that colonize cotton. 2.2. Minute pirate bugs: Orius tristicolor (Het.: Anthocoridae) is the most commonly found species in California cotton. They appear early in the season with both nymphs and adults feeding on a variety of small insects and eggs, though their main food source is thrips. 8 Biological Control of Key Pests in Cotton 2.3. Lacewings: Larvae of Chrysoperla carnea, C. comanche and Chrysopa nigricornis (Neur.: Chrysopidae) are the important lacewing predators in cotton. In the San Joaquin Valley large populations can also be found in alfalfa fields. However, in cotton, intraguild predation of lacewing larvae by other general predators prevents large populations from occurring (Anon. 1996). 2.4. Assassin bugs: The most common assassin bugs in California cotton fields are Zelus renardii and Sinea diadema (all regions), and S. confusa and S. complexa (desert valleys) (Het.: Reduviidae). Both nymphs and adults feed on insect prey, and assassin bugs can be found in cotton during mid and late- season (Anon. 1996), though high densities do not occur (Van den Bosch and Hagen 1966). 2.5. Damsel bugs: The damsel bug most commonly found in California is Nabis americoferus (Het.: Nabidae). In the desert valleys, N. alternatus is also commonly found. Adults and nymphs both prey on insects. (Van den Bosch and Hagen 1966) 2.6. Collops beetles: In the San Joaquin Valley, Collops vittatus occurs, while in the desert valleys C. marginellus (Col.: Melyridae) is common. Both species feed on moth eggs, aphids, mites and young caterpillars. While they can be found in cotton at any point during the season their populations do not build up until mid-season (Van den Bosch and Hagen 1966). 3. Lygus Bug: Lygus hesperus (Het.: Miridae) 3.1. Lygus Species and Damage 3.1.1. Description of pest The four species of lygus bug inhabiting cotton in the western United States are L. hesperus, L. elisus, L. desertinus and L. lineolaris. L. hesperus occurs most often in California and as a result is the most damaging. Under field conditions a female lygus lays an average of 50 eggs (Cave and Gutierrez 1983), and typically three generations occur per year in cotton (Anon. 1996). Lygus hesperus can feed on a wide variety of host plants, although it has a strong host preference for alfalfa, as well as other leguminous plants (Scott 1977). Other crop hosts include, but are not limited to, sugarbeet, tomato, beans and potato (Godfrey et al. 2005). When these other host plants become unsuitable (mature, dry or are harvested) for lygus, they will migrate into cotton. In California, safflower, alfalfa and weeds (including redroot pigweed, lambsquaters, knotweed, wild sunflower, shepherds purse, London rocket and black mustard) are important source populations for lygus infestations in cotton (Leigh and Matthews 1994, Anon. 1996). Lygus can feed on apical meristematic tissues, squares, and developing seeds. Meristem feeding can stimulate secondary vegetative growth, giving plants a bushy appearance (Leigh and Matthews 1994). Economic damage usually occurs when smaller squares are fed upon causing them to abort (Anon. 1996, Leigh et al. 1988). In the San Joaquin Valley, 4th and 5th instars have been shown to have greater impact on square damage and square loss than adults (Zink and Rosenheim 2004). Feeding on larger squares can lead to boll deformation, and high lygus densities can lead to feeding on bolls and yellow staining of the lint (Leigh and Matthews 1994). Migrations of large lygus populations from preferred hosts usually occur in June when cotton plants are most vulnerable (Godfrey and Leigh 1994). 3.1.2. Damage In 2003, lygus destroyed 26,862 bales of cotton and caused 268,222 acres to be treated with insecticides in California (Williams 2004). However, lygus damage can vary year to year as evident by the modest 9 Biological Control of Key Pests in Cotton amount of damage occurring the previous year (174 bales lost in 2002) (Williams 2003). The severity of lygus damage in cotton depends on rainfall patterns and availability of alternate hosts (Goodell 1998). Lygus can pose a threat to cotton in all growing regions of California, though it is usually a lesser problem in the desert valleys (Goodell and Toscano 2002). 3.1.3. Treatment thresholds Current treatment thresholds in the San Joaquin Valley are based on sweep net counts and stage of crop development. Treatment is recommended for 2-4 lygus bugs per 50 sweeps during early squaring, 7-10 per 50 sweeps at mid squaring, and 10 per 50 sweeps at late squaring (Anon. 1996). 3.2. Lygus Biological Control 3.2.1. Current parasitoids, predators and pathogens Anaphes iole (=ovijentatus, Hym.: Mymaridae), an egg parasitoid of lygus bug, is found in all cotton growing regions of the western United States (Anon. 1996). In Arizona cotton, mean monthly rates of egg parasitism by A. iole range between 0 and 36% (Graham et al. 1986). Leiophron uniformis (Hym.: Braconidae), a nymphal parasitoid, is found in the desert valleys (Anon. 1996). Monthly rates of parasitism by L. uniformis range from 0 to 10.6% in Arizona alfalfa (Graham et al. 1986). The most important predators of lygus eggs and nymphs are the big-eyed bugs, other predators include damsel bugs and collops beetles. Crab spiders will also attack lygus adults (Anon. 1996). There is little information on the impact of the generalist predators, although Leigh and Gonzalez (1976) carried out field cage studies to evaluate predation of lygus in California cotton. They found G. pallens to be effective against eggs and nymphs, while C. carnea provided no control. Surveys in the San Joaquin Valley found the entomopathogenic fungus Beauveria bassiana infecting L. hesperus populations. Infection levels were greater than 50% in some samples. Isolates of B. bassiana from this study are reported as currently in culture and under study for possible future release (McGuire 2002, 2003). 3.2.2. Classical biological control In 1998, parasitoids from related lygus bugs in Europe began to be imported and released into California for control of L. hesperus. In the summers of 1999, 2000 and 2001 adults and larvae (in lygus nymphs) of Peristenus stygicus and P. digoneutis (Hym.: Braconidae), both nymphal parasitoids, were released in several California locations. Overwintering recoveries of P. stygicus were made in 2000 and 2001, though no P. digoneutis were recovered. At one release site a maximum parasitism rate of 34% was recorded (Pickett et al. 2002). PCR primers have been developed to aid the identification of parasites in lygus nymphs (Erlandson et al. 2003, Zhu et al. 2004), and although hyperparasitism is not yet known in California, it has been detected in the northern part of the continent where the parasitoid P. pallipes is dominant (Ashfaq et al. 2005). 3.2.3. Augmentative biological control Although augmentative releases of A. iole have been shown to have some impact on lygus populations in strawberries in California (Udayagiri et al. 2000a), no comparable studies have been carried out in cotton. While lygus eggs may be more vulnerable in cotton than in strawberry (Udayagiri and Welter 2000b, Jackson 2003), and some elements of a mass rearing system have been developed (Jones and Jackson 1990, Riddick 2004), the cost of parasitoid production and their availability of sufficient material for 10