Pheromone Mating Disruption Offers Selective Management Options for Key Pests

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REVIEW ARTICLE t Pheromone mating disruption offers selective management options for key pests

Stephen C. Welter Carolyn Pickel Jocelyn Millar Frances Cave Robert A. Van Steenwyk John Dunley t

The direct management of insect pests using pheromones for mating disruption, or “attract and kill” approaches, can provide excellent suppression of key lepidopteran pests in agriculture. Important successes to date include codling moth in pome Pheromones are used by insects (and numerous other species) to communicate. fruit, oriental fruit moth in peaches When these messages are disrupted, pest insects fail to reproduce and mate. A sprayable formulation of microencapsulated pheromone is applied by helicopter. and nectarines, tomato pinworm in vegetables, pink bollworm in cotton and omnivorous leafroller in vine- huge expanses of forests or plantations, However, the correction of the blend yards. Large-scale implementation to the regional disruption of mating eliminated the problem (Mochizuki et projects have yielded significant re- processes by pests, to smaller “attract al. 2002). and kill” approaches in specific fields. A key benefit of pheromone-based ductions in pesticide use while main- While many different groups of insects programs is that they are highly selec- taining acceptably low crop-damage use pheromones, most successes to date tive. Typically, only the primary target levels. Because of some difficulties have been with lepidopteran pests (but- species responds to the pheromone, and with high populations of pests, these terflies and moths); these successes have nontarget effects on biological control programs should not be viewed as allowed for more biologically intensive agents within a field or outside of a stand-alone strategies but rather as approaches to control pests. cropping system are not observed. The use of pheromones against key pests one tactic within a suite of integrated Advantages and disadvantages pest management options. does not result in outbreaks of second- Many advantages of pheromone- ary pests or pest resurgence, creating based pest management systems are opportunities for the biological control heromones, defined as chemicals common to other biologically based of other pest species. secreted externally by an organism management approaches, including However, the high degree of selectiv- Pto send information to members of the virtually no detectable residues for ity may also be a significant obstacle same species, are used extensively by some dispensing systems, negligible to large-scale implementation, in cases insects to communicate with each other. health risks, a more rapid registration where secondary pests become a prob- Pheromones may signal information process and no accumulation in wildlife lem as insecticides are eliminated. as diverse as the sexual receptivity of or groundwater. Additional benefits Insecticide applications targeting the the producer, perceived dangers or the include reduced worker re-entry or pre- key pest sometimes inadvertently con- dominance of an individual in a colony. harvest intervals and limited impacts trol other pests as a collateral benefit. Researchers have interfered with these on other management practices, such as For example, outbreaks of leafrollers communication systems as a means to irrigation scheduling. Pheromone-based (such as Pandemis pyrusana) have been selectively control or manage pest spe- mating disruption has also been identi- reported in California apple orchards cies in agricultural and forest systems. fied as a strong tool for managing insec- utilizing pheromone-disruption pro- A variety of approaches employ ticide resistance. Whereas resistance to grams to control codling moth without pheromones to manipulate or disrupt pheromones applied over broad areas organophosphates (OPs)(Walker and the natural behaviors of insects, such might be expected, there is only one Welter 2001). Similar results were seen that population levels are reduced and documented case of resistance, when an in apple orchards under a variety of crop damage diminishes. These strate- incomplete pheromone blend was de- programs using the mating disruption gies include mass trapping efforts over ployed against the tea tortrix in Japan. of codling moth (Nicholas et al. 1999);

16 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 Pheromones may signal when the OP azinphos-methyl was re- vent moths from locating traps. Even in information as diverse as moved, populations of the wooly aphid conventional fields, pheromone traps the sexual receptivity of (Eriosoma lanigerum), lightbrown apple are rarely used as the sole indicator of moth (Epiphyaas postvittana), San Jose pest problems; rather, they are often the producer, perceived scale (Quadraspidiotus perniciosus) and used in combination with other ap- dangers or the dominance budworm (Helicoverpa spp.) increased. proaches, such as direct damage as- Other possible limitations include: (1) sessments. The use of high-dose lures of an individual in a colony. the lack of an identified pheromone for that still attract some moths even under Researchers have interfered some pest species; (2) high development mating disruption has proven useful with these communication and production costs; (3) requirements for tracking the flights of some pests for specialized application techniques or (such as codling moth) or as a supple- systems as a means to equipment; and (4) the need to supplemental risk-assessment tool. Other spe- selectively control or ment the pheromone program in high cies, such as oriental fruit moth (Cydia pest-pressure situations. Pheromone molesta), do not exhibit this response. manage pest species. programs are most effective with low to However, it may be possible to develop moderate population densities, whereas nonpheromonal attractants for use in high-pressure situations in which dam- mating disruption (Light et al. 2001). logical factors behind these successes age from previous years exceeded 1% to appear to be the relatively long life and Approaches in the field 2% often require supplemental insecti- slow reproductive rate of the weevils, cide applications to prevent commercial Mass trapping is a direct control and the fact that the aggregation phero- damage. Treatment thresholds have strategy in which large numbers of mones attract both sexes. Success is been developed using modified phero- pests are captured and removed. This critically dependent on efficient mass- mone lures, but they vary between strategy has been successful in control- trapping to remove weevils faster than crops and regions. Mating disruption, ling large weevils in tropical crops such they can reproduce. like most other pest management strat- as oil palms, palmito palms (grown for In situations with other insects that egies, needs to be viewed within the hearts of palm), plantains and bananas. do not have these biological character- context of an entire pest management In oil palm plantations in Central and istics, and particularly with sex phero- system rather than as a stand-alone pro- South America, the palm weevil (Rhyn- mones that only attract one sex, mass gram. cophorus palmarum) is a vector of the trapping is generally less effective de- Monitoring the target pest with lethal red ring nematode. Pheromone- spite some larger projects collecting bil- pheromone traps also can become based mass trapping using one trap per lions of individuals (Ryan 2002). It has problematic, because the pheromones acre is now the principal control method been successful with smaller or confined used to disrupt mating will also pre- (Oehlschlager et al. 2002). The key bio- populations such as those found on islands (the sugarcane wireworm [Mela- notus okinawensis]) or with small, local- ized infestations of introduced pests

Jack Kelly Clark Kelly Jack targeted for eradication efforts, such as the white-spotted tussock moth (Orgyia thyellina) in New Zealand. Pheromone-based mating disruption, which is the most commonly used approach, may work via a number of overlapping mechanisms that interfere with mate location and reproduction. Obviously, if males are prevented from locating or copulating with sufficient numbers of females, pest populations

Jack Kelly Clark Kelly Jack will decline. This approach works without the direct mortality of target individuals, preventing offspring and subsequent damage. Attracticides, or “lure and kill” strategies, combine an attractant with an insecticide, eliminating individuals that contact the lure. Many limitations of mass trapping also apply to programs By carefully monitoring crop damage and insect populations, and applying pheromones to disrupt mating, growers have successfully protected orchard crops from insect pests. that target males only. Depending on Left, former UC staff researcher Jeannine Lowrimore counts codling moths in a trap; how the system is implemented, it may top right, shoot-strike damage; bottom right, male peachtree borers in a pheromone trap. also interfere with the male’s location of

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 17 tion of mechanisms including camouflage, competition between pheromone dispensers and females, habituation, and some advancement of the rhythm of the male’s response to the female’s Pheromones can be applied pheromone, which may result in asyn- using a variety of dispens- chrony in sexual behaviors. ers, including (clockwise The use of antagonistic compounds, from top left): microen- agonists, pheromone mimics and syner- capsulated pheromones, sprayed like insecticides; gists is broadly grouped under the term hand-applied dispensers, parapheromones, loosely defined as an- with a reservoir and perme- thropogenic compounds structurally re- able membrane to regulate lated to natural pheromone compounds release; hollow fibers; and twist-tie ropes. that affect the behavior or physiology

Jay Brunner/Wash. State Univ. Brunner/Wash. Jay of the insect’s communication system (Renou and Guerrero 2000). This group females through false trail-following, as nisms of mating disruption. Sensory includes compounds of plant origin well as the primary effect of the male’s adaptation is a reduction in the firing used to annihilate (with an attractant attraction to insecticide-laced baits. rates of the sensory structures after plus a lethal agent) the males of impor- prolonged exposure to the pheromone, tant dipteran pests, such as bait sprays Mechanisms of mating disruption whereas habituation is a reduction in for fruit flies or walnut husk flies. While Limitations to developing mating the insect’s response to the pheromone parapheromones alter neural activity, disruption programs include a lack of due to some change in the central ner- change insect behaviors and depress or understanding about the mechanisms of vous system. Both of these mechanisms synergize trap capture, their utility in mating disruption for different types of can generate the same nonresponsive the field for management purposes has dispensers, the biological or behavioral outcome. Different species respond received limited testing and remains characteristics of the target pest, and differently to prolonged exposures in highly variable. how pheromones move and distribute pheromone-treated fields. Habituation, However, studies have also shown themselves within agricultural systems which may result in arrested movement, that even in programs with minimal (Cardé and Minks 1995; Sanders 1997). has been proposed as a possible mecha- crop damage, significant mating may Surprisingly, the principle mechanisms nism for high-dose exposures from still occur. Alternative mechanisms are of action for even some of the most suc- devices that periodically release phero- being explored that focus on the effects cessful programs (such as codling moth mones in large aerosol puffs (puffers), of delaying mating rather than its com- in pome fruit) are unclear. or in close proximity to passive dispens- plete suppression. Delays in mating by Researchers have shown that the ers. Both can occur with either complete virgin females or males has been shown pheromone plume is not a uniform or partial pheromone blends. in multiple species to result in depressed cloud, but rather a series of filaments of The camouflage of a female’s phero- egg-laying and increased sterility of the pheromone interspersed with pockets mone plume presumes that the overlap- eggs laid (Jones and Aihara-Sasaki 2001; of zero to low concentrations due to ping plumes from multiple pheromone Fadamiro and Baker 1999). Therefore, natural turbulence in the air (Sanders dispensers generate a “fog” of phero- exclusive focus on the complete preven- 1997). The male is exposed to a series of mone, so that the males can no longer tion of mating may not be warranted. rapidly changing concentrations, which distinguish the pheromone emitted by Mating disruption still remains a useful requires both the interpretation of the a female from the elevated background. term if disruption is to include both the odor and a resetting of the antennal re- The false-trail-following mechanism prevention of mate location and mating, ceptors within milliseconds to perceive produces direct competition between and factors that interfere with or delay the next pheromone molecule (Leal calling females and synthetic dispens- the normal mating processes. 2003). The male proceeds to fly upwind ers, as males spend time and energy Pheromone-dispensing technologies in a series of surges interspersed with locating “false females.” This diversion crosswind casting when it detects pock- of the male’s activities results in either A variety of dispensing technolo- ets of air with reduced concentrations a decrease in the proportion of females gies have shown promise and success of pheromone. For most species, a tur- mated or a delay in mating. under commercial conditions and are bulent plume with pockets of high and The proposed mechanisms by which now available to growers. Each varies in low concentrations is required for prop- mating disruption might work are not terms of ease of application, cost and the er upwind flight; if a column of air is mutually exclusive, and several mecha- mechanism of disruption. Challenges for filled uniformly with pheromone, then nisms may be important for the same pheromone dispensers include protect- the sensory structures may fatigue and insect under different conditions. For ing components from degradation by no longer respond to the pheromone. example, Cardé et al. (1998) demon- environmental factors and the uniform Sanders (1997) and Cardé and Minks strated that the mating disruption of the release over time of different types of (1995) have reviewed different mecha- pink bollworm occurs from a combina- compounds (such as aldehydes, alco-

18 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 hols or acetates) with varying chemical and physical properties. MECs. Microencapsulated pheromones (MECs) are small droplets of pheromone enclosed within a polymer capsule, which controls the pheromone release rate. The capsules are small enough to be applied as suspensions with the same commercial equipment used to spray insecticides. The effective field longevity of these materials generally ranges from days to weeks depending on climatic conditions, capsule size and properties, and the chemistry of the pheromone components. However, the material is applied directly to the com- Fig. 1. Downwind area of trap suppression by a single puffer with a 12-hour “on” cycle, modity, an important consideration in placed in a walnut orchard coincidental with the release of a uniform grid of sterile, food crops. marked codling moth. Number of moths is 5-day cumulative trap-catch total. Hand-applied dispensers. Larger, hand-applied dispensers include sys- of pheromone from the fiber, this tech- Current uses to control insects tems with an impermeable reservoir nology has a relatively constant emission fitted with a permeable membrane for rate over time. These fibers are often Pheromone-based devices have regulating pheromone release, and combined with an adhesive material dur- achieved the successful control of analogous laminate dispensers that con- ing application and may require special- insect pests in almost all types of agri- sist of a central pheromone-containing ized ground or air equipment to apply. culture, including perennial orchards, core sandwiched between two poly- High-emission dispensers. High- vineyards, annual vegetables and fiber mer films. These dispensers can be cut emission dispensers were developed crops. The following five insect pests into various shapes and sizes ranging to emit larger quantities of pheromone have enjoyed historical and recent suc- from larger, hand-applied dispensers and use fewer dispensers per acre to cut cesses with pheromone-based manage- to smaller, confetti-like flakes that can down on labor costs (Shorey and Gerber ment systems. be applied by specialized ground or air 1996; MafraNeto and Baker 1996). The Codling moth. A recent success in- applicators. Pheromones can be mixed only commercially available dispenser volves the management of codling moth into paraffin wax or aqueous paraffin of this type at this time is the Suttera in pear and apple orchards in California emulsions and applied directly to the puffer. The puffer uses a pressurized and the Pacific Northwest (Calkins and tree using hand-dispensers (Atterholt aerosol can filled with a pheromone, Faust 2003)(fig. 2). In 2001, the mating et al. 1999) or potentially in modified which dispenses metered puffs of pher- disruption of codling moth was used sprayers. omone at fixed time intervals (such as on about 135,000 acres of pome fruit, or Hand-applied dispensers also in- every 15 minutes). The number of units roughly 45% to 50% of the acreage from clude pheromone-impregnated poly- per acre varies depending on orchard the Sacramento Valley to the Pacific mer spirals, and twist-tie “ropes” that size and patterns of distribution, but ap- Northwest. Adoption rates in southern consist of a pheromone-filled plastic proximately one-half to one dispenser tube with a wire spline along one side. per acre is typical for codling moth in The wire allows these dispensers to be pears. twist-tied directly to the plant or hung Recent research attempting to de- indirectly with a clip. New technolo- fine the effective area of trap suppres- gies using alternative “rope dispensers” sion of codling moth, using uniform without a spline have been developed releases of sterile moths, revealed a as well. The larger reservoirs of the surprisingly long plume that was typi- hand-applied dispensers (ropes, lami- cally greater than 1,500 feet long and nate systems, spirals) allow for effective between 300 and 500 feet wide (fig. 1). lifetimes of 60 to 140 days, such that In addition, researchers are beginning single applications early in the season to test the possibility of using large, Fig. 2. Codling moth pheromone applications may suppress mating all season. passive-release devices consisting of in California in walnuts, apples and pears. To Hollow fibers. Hollow fibers have polymer bags loaded with large doses show use trends rather than absolute rates, been employed since the 1970s in mat- of pheromones (Mahr and Baker 2001). data includes all delivery technologies and ing disruption programs. The fibers These devices are intended to work in multiple applications to the same acre within a year. Sources: UC Integrated Pest Manage- consist of a short, impermeable plastic the same general way as puffers, but ment Web site, www.ipm.ucdavis.edu; Cali- tube that is sealed at one end and filled with no batteries or moving parts they fornia Department of Pesticide Regulation with pheromone. After an initial burst are potentially more reliable. pesticide-use tracking data.

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 19 In Lake County, 15 pear growers uti- lized high-dose “puffer” dispensers on about 1,300 acres. The high-dose aerosol cans, inset, are hung high in trees, releasing the pheromones at regular intervals.

insecticide programs were failing because of extraordinary levels of resistance that jeopardized the whole industry by the late 1980s (Trumble 1997). Some damage suppression was achieved in cherry tomatoes, but damage levels were still variable and excessive in both conventional insecticide and pheromone-treated plots. A pest management program was developed to address resistance issues and provide a more sustainable system, while considering its overall economics. For apple-growing regions are lower due to for codling moth was reduced 75%, winter and spring plantings, conven- higher pest population levels, presum- from an average of four to approxi- tional sites suffered excessive damage ably the result of more generations per mately one per season. of 75% to 90%, while damage was re- year. While the dominant release device This pattern was repeated with four duced to 33% to 35% in the IPM plots. from 1995 to 2000 was hand-applied additional areawide sites, initiated by Overall economic evaluations dem- dispensers (Isomate C+ rope dispensers a team of entomologists from UC, Or- onstrated substantial economic returns and Checkmate CM laminate dispens- egon State University, Washington State from the IPM program compared to ers), others such as puffers were suc- University and the U.S. Department conventionally treated plots. Phero- cessfully used on more than 1,300 acres of Agriculture’s Agricultural Research mone treatment remains relatively local of pears in Lake County. Service in Wapato, Wash. Ultimately, 17 and site-specific in California given that The use of mating disruption in additional sites were established in four tomato pinworm is a greater pest in pome fruit accelerated after the de- Western states. Although the areawide fresh-market than processing tomatoes. velopment of the first such areawide research programs are no longer ac- Newer products, including hand-applied program in the Randall Island region tive, the infrastructure and momentum or sprayable formulations, have been of the Sacramento River Delta in 1993. developed have allowed the approach introduced. However, the use of the Five growers and their pest control to flourish. Studies have shown that tomato pinworm mating-disruption advisors committed 760 contiguous codling moth also can be controlled in program was fairly flat from 1995 until acres to a long-term program to reduce walnuts with hand-applied dispens- 2000, when an increase occurred (fig. 4). codling moth populations over time, us- ers in smaller, more limited trials, but Pink bollworm. Pink bollworm ing a combination of mating disruption program costs were higher than con- (Pectinophora gossypiella) has been the and reduced insecticide. Codling moth ventional programs given the high costs target of an intensive, long-term and populations in an organic apple orchard of application to larger-canopied trees successful mating-disruption effort directly across the river plus additional (Grant et al. 2003). A similar result was (Staten et al. 1997) in both the United conventional sites were used for com- achieved in an areawide program in States and abroad. A variety of strate- parison. Lake County by Cooperative Extension, gies have been employed, including In the Randall Island project, popu- local pest control advisors and growers applications of hollow fibers, chopped lation levels in pheromone-treated using pheromone “puffers” on more laminate flakes, sprayable microencap- areas — as documented by mean trap than 1,300 acres owned by 15 growers. sulated pheromone, twist-tie ropes or counts — were reduced over the 6-year Tomato pinworm. The mating dis- laminate membrane dispensers. Prob- period to less than 10 moths per trap ruption of tomato pinworm (Keiferia lems with successful mating disruption from highs of about 80 moths per trap lycopersicella) was originally developed in fields with high moth populations (fig. 3). Fruit damage was held to less using hollow fibers in the 1970s and were detected and supplemental control than 1% in all years with final damage 1980s (Van Steenwyk and Oatman tactics were used. Combinations of ster- levels for 1998 to 1999 of less than 0.1%. 1983). It has been particularly suc- ile insects and mating disruption were The number of insecticide applications cessful in Mexico, where conventional implemented in large-scale programs in

20 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 the Imperial and Mexicali valleys. the introduction of Bt cotton, except in Successful mating disruption in areas under the pink bollworm eradica- the late 1980s in the Coachella Valley tion program that are not using trans- resulted in significant decreases in in- genic cotton. secticide use (7.3 applications in 1985 Oriental fruit moth. Mating dis- to no treatments in 1988). However, ruption has been used worldwide to the immigration of mated moths from control oriental fruit moth in stone the Imperial Valley to the Coachella fruit, peaches and nectarines using both Valley in 1989 appears to have resulted hand-applied and sprayable formula- in decreased program efficacy. The tions (Pickel et al. 2002). In 1995, a series isolation and areawide suppression of of replicated field plots was established Fig. 5. Oriental fruit moth pheromone appli- populations improved the efficacy of in California to evaluate three hand- cations in California peaches and nectarines. the mating disruption program, similar applied dispensers (laminate, mem- Data from DPR includes all delivery technologies and multiple applications to the same to later experiences with codling moth. brane and rope dispenser) in peach acre within a year. Sources: see figure 2. A recent, interesting twist is the intro- orchards. Season-long control was duction of transgenic cotton with the achieved, with approximately 34% Bt gene, which has been reported as of the orchards having no detectable restricted. Sprayable formulations may highly effective against pink bollworm. damage and 63% having less than 3% be preferable to address more-local or Mating disruption has declined with damage, the current processor standard. less-severe infestations of omnivorous However, typically one orchard out of leafrollers, a pest that is unpredictable 21 in each year had damage in excess of in distribution and severity. 3%, which again reinforced that mating Future directions disruption in orchards with high moth populations needs to be supplemented While mating disruption provides with other control strategies. Overall an excellent management option for re- full-season costs for the pheromone pro- ducing insecticide use, it often requires gram were significantly higher than for supplemental insecticides to control conventional treatments, such that grow- high pest populations. The successful ers developed a modified program using implementation of mating disruption a single application of the hand-applied will require curative, rapid treatments pheromone dispensers supplemented to address increasing or unexpected with insecticides later in the season. The population surges. As outlined in partial pheromone program appears to Metcalfe et al. (2002), the implications be more cost effective at this time. of eliminating OP insecticides will More recently, both puffer-type dis- depend on the existence of alternative pensers and sprayable microencapsu- strategies, yet the implementation of Fig. 3. Codling moth (A) trap totals and (B) lated formulations have seen some use. pheromones may also require devel- damage levels for the season in pheromone- treated plots in the Randall Island project. Oriental fruit moth is an easily disrupt- opment of selective insecticides as ed pest, resulting in a large increase in supplements. applications from 1995 to 2000 (fig. 5). Programs are being developed to Increased adoption rates will depend address other lepidopteran pests in on growers’ perception of risk from systems for which the key insects may oriental fruit moth, the availability of be managed by pheromones or other se- effective, less expensive insecticide lective management tools. As key pests alternatives, and the complex of pests like codling moth come under control, within the orchard. research is under way to improve the Omnivorous leafroller. The mating mating disruption of other orchard disruption of omnivorous leafroller pests, such as the oblique-banded with hand-applied or sprayable formu- leafroller (Choristoneura rosaceana) and lations has increased since 1998 in Cali- Pandemis leafroller (Pandemis pyrusana). Fig. 4. Tomato pinworm pheromone use in fornia vineyards, with more than 35,000 Research is also ongoing in programs California for processing and fresh-market acre-applications made. Given that this that have had partial success, such tomatoes. Data from DPR includes all delivery technologies and multiple applications pest is only important in the state’s as for navel orangeworm (Amyelois to the same acre within a year. Sources: see warmer grape-growing regions, the transitella). Opportunities with stored- figure 2. need for pheromones is geographically product pests such as the Indian meal

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 21 moth (Plodia interpunctella [Hubner]) or References Sacramento, CA. 41 p. + app. http://www. Angoumois grain moth (Sitotroga ce- cdfa.ca.gov/publications.htm Atterholt CA, Delwiche MJ, Rice RE, Millar JG, Daane KM, McElfresh JS, et realella) are being explored (Fadamiro Krochta JM. 1999. Controlled release of in- al. 2002. Development and optimization and Baker 2002). While most suc- sect sex pheromones from paraffin wax and of methods for using sex pheromone for cesses have been with lepidopteran emulsions. J Controlled Release 57:233–47. monitoring the mealybug Planococcus ficus insects, research in other insect orders Calkins CO, Faust RJ. 2003. Overview of (Homoptera: Pseudococcidae) in California areawide programs and the program for sup- vineyards. 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