REVIEW ARTICLE ▼ Biological and cultural controls… Nonpesticide alternatives can suppress crop pests

Nicholas J. Mills Kent M. Daane ▼

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

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

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

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

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

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

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