REVIEW ARTICLE t Microorganisms and their byproducts, nematodes, oils

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

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

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

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

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

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

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

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

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

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

38 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 fornia in 2001. Pyrethrins are produced by certain species of chrysanthemums. The natural pyrethrins are contact poisons, which quickly penetrate the cuticle to the insect’s nervous system. A few minutes after exposure, insects are paralyzed. This quick knockdown is one of the strong attributes of pyrethrins. However, enzymes in the insect swiftly detoxify the natural pyrethrins and some pests will recover. To delay the en- zyme action so a lethal dose is assured, OPs, carbamates or synergists may be Above, in 1915 a worker sprayed dry sulphur added. The short residual activity of py- on young prune trees infected with brown rethrum on plant surfaces allows crops mite near Yuba City. Today, sulfur is still widely used as a pesticide to control mites on to be harvested shortly after application. grapes, citrus and other crops. Right, an air- Azadiractin. Azadiractin is extracted blast sprayer with tower treats citrus crops from seeds of the neem tree (Azadirachta with petroleum-based oils to control citrus indica). Chemically, azadiractin falls red mite and California red scale. within a class of compounds known as tetranortriterpenoids. The properties of applied as a baited toxicant for citrus Petroleum oils and particle films these insecticidal compounds include thrips and avocado thrips. Activity is feeding and ovipositional deterrence, affected by the percentage of alkaloids Petroleum-based oils have been used repellency, growth disruption, reduced in the extracted product and by the pH for a number of years to control insect fitness and sterility in a number of in- of the water used for the application. pests, especially mites and scale insects. sect species. The active ingredient is Because of sabadilla’s variability in Early formulations caused several prob- structurally similar to insect hormones activity for thrips control and its rapid lems because they had components that called ecdysones, which control meta- breakdown in light, spinosad and abam- were phytotoxic to plants. More recently, morphosis. Therefore, the disruption of ectin have largely replaced it in citrus petroleum oils have become highly re- the insect’s development and molting and avocado. However, when thrips fined and rarely show phytotoxic effects. process (interfering with their life cycle) develop resistance to spinosad and Their common distillation points are is likely to follow exposure. abamectin, as citrus thrips has to OPs, 415 and 440. The heavier 440 oils show Azadiractin is primarily used to con- carbamates and pyrethroids, interest in greater efficacy, but also more potential trol whiteflies, aphids, thrips, fungus sabadilla is likely to resume. for phytotoxicity. The 440 oils tend to be gnats, mealybugs, leafminers and other Other plants. Several other plants used in fruit and nut trees as dormant arthropods on food, greenhouse crops, produce compounds that are reportedly applications for mites and lepidopterous ornamentals and turf. Its acceptance toxic to arthropods. Cinnamaldehyde, and armored scale pests, often in combi- and usage in conventional agriculture derived from cinnamon oil, is the toxic nation with other pesticides. The lighter have been low, however, due to its er- element in the product Cinnamite. This 415 oils are used for in-season treatments ratic performance on major-crop insect product controls mites and aphids, as alone or in combination with other pes- pests. The more extensive use of this well as powdery mildew, on a range of ticides such as spinosad and abamectin. product in conventional agriculture is crops. Oils of rosemary, wintergreen, In citrus, 0.5% to 2% oil is used in spring limited by its narrow application win- clove, garlic and lemon are also sold and for citrus red mite (Panonychus citri) dow (during the susceptible life stage), reported to have insecticidal properties. and in the summer as a 1.4% spray for the need for frequent applications and a Certainly as insects and plants coevolved, California red scale (Aonidiella aurantii). narrow pest spectrum. plants developed defense compounds to Phytotoxicity can be avoided by treat- Rotenone. Rotenone is a nonspecific ward off attack by these herbivores. The ing during the coolest periods of the day insecticide with some acaricidal proper- isolation of these compounds could pro- and ensuring that the orchard is well ir- ties, which is used for pest control in vide useful crop-protection tools in the rigated prior to treatment. a variety of crops. It is extracted from future, but they are not cost effective in Presently, one product is available in several plants in the pea family. Because commercial agriculture today. the mineral-based particle film category. of its toxicity to aquatic animals, espe- Inorganic products. For arthropod Kaolin (Surround) is a naturally occur- cially fish, it should not be used near control, sulfur is the most commonly ring product, generally inert to mam- waterways. used inorganic product. Sulfur has mals, which does not react with other Sabadilla. Sabadilla is extracted from strong fungicidal properties and sec- materials (Glenn et al. 1999). When used seeds of the Mexican lily (Schoenocaulon ondarily controls spider mites. Sig- as a pesticide, kaolin is sprayed as a officinale), which contain the alkaloid nificant usage for spider mite control powdered suspension on crops, where veritrine as the active ingredient. It occurs annually on grapes, citrus, orna- it forms a barrier film that repels and is mixed with sugar or molasses and mental plants and cotton. prevents target pests from penetrating

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

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