biological control of arthropod pests: traditional and emerging technologies

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Biological control of arthropod pests: Traditional and emerging technologies

Marjorie A. Hoy

American Journal of Alternative Agriculture / Volume 3 / Issue 23 / January 1988, pp 63 68DOI: 10.1017/S0889189300002198, Published online: 30 October 2009

Link to this article: http://journals.cambridge.org/abstract_S0889189300002198

How to cite this article:Marjorie A. Hoy (1988). Biological control of arthropod pests: Traditional and emerging technologies. American Journal of Alternative Agriculture, 3, pp 6368 doi:10.1017/S0889189300002198

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Biological control of arthropod pests: Traditionaland emerging technologiesMarjorie A. Hoy

Abstract. Biological control of arthropod pests has a long history of useful practicalapplication. Parasites, predators, and pathogens have been employed in many cases tocontrol pest arthropods in an efficient, cost-effective, and permanent manner. Thetraditional tactics used in biological control (classical, augmentation, and conservation)remain vital and valuable tools in the biological control of pests for agricultural crops,range lands, forests, and glasshouses. New technologies offer promise. One emergingtechnique involves the genetic improvement of natural enemies of arthropods throughselection, hybridization, or recombinant DNA technology.

Key words: biocontrol agents, improvement, selection, hybridization, recombinantDNA technology, forests, rangelands, farmlands

Introduction

Crop yields in the United States arereduced by the impact of a variety ofpests. Weeds are potentially the mostdamaging, followed by approximately8000 species of insects and at a lowerlevel by plant pathogens and nematodes(Batra, 1982). Control of pest insects hasbeen achieved through chemical, cul-tural, and biorational controls, but bi-ological control has unique advantagesover the other tactics.

Biological control has been defined asthe "actions of parasites, predators, andpathogens in maintaining another or-ganism's density at a lower average thanwould occur in their absence" (DeBach,1964). Some scientists would includehost plant resistance, autocidal control,and pheromones under the category ofbiological control, but, while these bior-ational approaches to pest control havea biological basis, many investigators do

Presented at Institute for Alternative Agriculture Sym-posium on Biological Pest Control, March 1, 1988, Wash-ington, DC.

Marjorie A. Hoy is Professor and Entomologist, De-partment of Entomology, University of California, Berke-ley, CA 94720.

not consider them to be biological con-trol. Generally, biological control hasbeen achieved by the use of one of threeapproaches-classical, augmentation, orconservation.

Classical biological control

"Classical" biological control is basedon the importation of exotic natural ene-mies (parasites, predators, or pathogens)and their long-term establishment in thenew environment, a strategy which maythen provide long-term control of thetarget exotic pest arthropod or weed.This approach to biological control hasbeen rewarding; hundreds of successfulprojects have reduced damage caused bya wide array of exotic pest arthropodsand weeds (Laing and Hamai, 1976;Clausen, 1978). In addition, once a suc-cessful program is achieved in one lo-cation, the same natural enemies arefrequently used to control the same pestselsewhere in other climatically similarlocations. Around the world, about 170successes were achieved between 1964and 1976 by introducing natural enemiesinto a second site after they had beenproven effective in the original geo-graphic site of introduction (Luck et al.,

1988). Natural enemy importation thusremains an important and effective tacticin pest management, particularly in themanagement of those arthropod andweed pests that are exotic. This ap-proach to biological control, unfortu-nately, has received less support than itdeserves.

While many scientists are worriedabout the extinction of animal and plantspecies in ecosystems, agricultural pestmanagement specialists are concernedabout additions to the fauna and floraof agroecosystems. In 1971, the U.S. De-partment of Agriculture established atask force to review the effectiveness ofplant quarantines in preventing the entryof exotic pests and to quantify the risksassociated with the entry of such pestsand diseases (Sailer, 1983). A list of im-migrant insects and related arthropodsin the United States was compiled thatcategorized the immigrants as pests,beneficial species, and those of no knowneconomic importance. The list continuesto grow as additional species are found.At the conclusion of the 1971-1972study, 1115 species were recognized tobe of foreign origin and this number hadincreased to 1385 by 1977. Sixteen insectorders, mites (Acarina), and spiders (Ar-aneae) are represented among the exoticarthropod species.

Foreign insect and mite species areconsidered to be responsible for a majorpart of all crop losses; one estimate isthat they are responsible for 50 percentof such losses in California (Sailer,1983). When viewed nationally, foreignspecies comprise 39 percent (235) of ap-proximately 600 important arthropodpest species. Another 630 foreign speciesare on the list as pests of lesser impor-tance, and an additional 420, or almost25 percent of the immigrant fauna, arespecies of no known importance, whilethe remaining 398 are in some degree

Volume 3, Numbers 2 and 3 63

beneficial (Sailer, 1983). Exotic invadersinclude such pests as the Japanese beetle,European corn borer, Florida red scale,Rhodesgrass scale, spotted alfalfa aphid,gypsy moth, cottony cushion scale, Cal-ifornia red scale, olive parlatoria scale,European red mite, imported southernred fire ant, Russian wheat aphid, andboll weevil.

Arthropods probably will continue tobe added to the fauna of the UnitedStates at the rate of about eleven speciesper year, despite the efficacy of the na-tional quarantine system (Sailer, 1983).Of the eleven, seven are likely to be pestsof some importance, and about everythird year a pest of major significancewill be discovered. Assuming that manyof these pests are not or cannot be erad-icated, classical biological control willremain of crucial importance in con-trolling new exotic pests in forests, rangelands, and agroecosystems.

Classical biological control has beenactively practiced for about 100 years inthe United States. Worldwide, approx-imately 2300 introductions directedagainst insect pests have provided com-plete biological control in about 100cases (Ehler and Andres, 1983). Sub-stantial control was provided in an ad-ditional 140 cases. Estimates of projectoutcomes that are successful range from16 to 34 percent. Many factors affectsuccess in classical biological controlprograms, including climate, naturalenemies, habitat type, genetics, hostcompatibility, host phenology, and op-erational procedures. Thus, while clas-sical biological control is effective andhas yielded complete and lasting controlin many important situations, there areseveral aspects of this pest managementtactic that require additional research(Ehler and Andres, 1983; Hoy, 1985a).As noted by Huffaker (1971), "Manyattempts have been only casual or haveinvolved use of a particular natural en-emy against unsuitable species or in un-suitable environments. The possibilitiesfor controlling the notorious codlingmoth in this way, or the Mexican beanbeetle, or the cotton boll weevil, for ex-ample, have only been explored super-ficially."

There are many views as to what theresearch priorities in classical biological

control should be. There is little dis-agreement about the fact that this con-trol has been under-exploited and under-funded. In one sense, it has been over-sold; the dramatic cases in which com-plete biological control has beenachieved through a small investment inresearch funds has, in my opinion, re-sulted in unrealistic expectations as tothe resources needed to properly con-duct classical biological control pro-grams. This could be labeled the"cottony cushion syndrome."

The cottony cushion scale threatenedthe citrus industry in California in thelate 1800s. This exotic species was sus-pected to have come from Australia. Avery small amount of funding ($2000)was obtained to support a field agent'ssearch for natural enemies in Australiain 1888. A parasite and a small ladybeetle (then called Vedalia) were foundattacking the scale in the Adelaide areaof Australia, and 129 beetles wereshipped to California. There they wereplaced on a small infested citrus treeenclosed in a mesh tent in January, 1889.By early April the scales were controlledon the caged tree and by early June over10,000 beetles had been distributed tovarious southern California groves. Bythe end of 1889 the Vedalia beetle hadcleared the scale pest from hundreds ofacres of citrus. Unfortunately, most clas-sical biological control programs prob-ably require substantially more time andresources than were necessary for thisproject, yet such resources are rarelyprovided. However, if they were pro-vided, both the rate of establishment andrate of success in classical biological con-trol of arthropod pests and weeds couldprobably be increased, thus providinglong-term, economical, and environmen-tally sound control of exotic pests (Huf-faker, 1971; Tauber et al., 1985).

Augmentation

Augmentation involves efforts to in-crease populations or beneficial effectsof natural enemies of both native andexotic pests (Rabb et al., 1976). A com-prehensive review of augmentation in bi-ological control is found in Ridgway andVinson's (1977) book on Biological Con-

trol by Augmentation of Natural Ene-mies. Augmentation involves varioustechniques, including periodic releasesand environmental manipulation. Peri-odic releases may be labeled inundativeor inoculative, depending upon the num-bers of natural enemies released and theinterval during which they are expectedto provide control. Environmental ma-nipulation may include provision of al-ternative, factitious hosts or prey, use ofsemiochemicals to improve natural en-emy performance, provision of environ-mental requisites such as food or nestingsites, and modification of cropping prac-tices to favor natural enemies. Augmen-tation has been particularly successfuljnglasshouse crops (Hussey and Scopes,1985).

Inundative releases are designed tocontrol a pest by the actions of the re-leased natural enemies, not by the ac-tions of their progeny, and thus can beconsidered "biotic insecticides." Inun-dative releases are currently hamperedby our limited ability to produce high-quality, inexpensive, mass-reared natu-ral enemies. Thus, advances in currentresearch on synthetic diets, artificicalhosts, quality control, and genetic ma-nipulation could result in increased useof this tactic (King and Leppla, 1984;Hoy, 1986).

Another emerging technology is theuse of semiochemicals to improve theefficacy of natural enemies in augmen-tation schemes. Parasitic insects use var-ious chemical cues to locate their hosts(Nordlund et al., 1981). Recent reportsindicate that learning can modify theresponses of parasites to these chemicals(Lewis and Tumlinson, 1988). The com-plexity of host seeking behavior exhib-ited by arthropod natural enemies is onlybeginning to be understood and couldlead to the more sophisticated use ofnatural enemy augmentation.

Conservation

Conservation involves protecting andmaintaining natural enemy populations.Conservation is crucial if both nativeand exotic natural enemies are to bemaintained in agricultural ecosystems.Most commonly, conservation involves

64 American Journal of Alternative Agriculture

modifying pesticide application prac-tices so that they occur only when thepest population exceeds specified levels.In some cases, conservation of naturalenemies can be achieved by changing theactive ingredient, rates, formulations,timing, and location of pesticide appli-cations (Hull and Beers, 1985). Or, ex-isting populations of natural enemies canbe protected by maintaining refuges. Ac-cording to Tauber et al (1985), "It isprobable that the most dramatic increasein the utilization of biological control inagricultural IPM systems could comethrough the judicious use of selectivepesticides in conjunction with effectivenatural enemies in specific cropping sys-tems, in specific geographic regions.While we have some knowledge of pes-ticide selectivity, it is woefully inade-quate to generally allow such preciseusage." As long as key pests cannot becontrolled biologically, culturally, orthrough host plant resistance, agricul-tural chemicals will be needed. Learninghow to conserve natural enemies in theagroecosystem is an effective way to in-crease the use of biological control inagriculture (Hull and Beers, 1985).

Emerging technologies

Genetic manipulation of natural ene-mies of arthropods offers promise of en-hancing their efficacy in agriculturalcropping systems. Genetic manipulationof other beneficial arthropods, such assilkworms and honey bees, has been con-ducted for hundreds of years (Hoy,1986). Such manipulation of biologicalcontrol agents seems to be a logical ex-tension of the domestication of cropplants and animals that has been part ofagriculture for thousands of years, sincemany agricultural systems are artificial.As in crop breeding, three potential ge-netic manipulation tactics exist, i.e., ar-tificial selection, hybridization (use ofheterosis), and recombinant DNA(rDNA) techniques. To date, only arti-ficial selection of arthropod natural ene-mies has been successfully employed,and the potential role of heterosis orrDNA technologies remains to be doc-umented (Hoy, 1985c, 1986; Beckendorfand Hoy, 1985).

Identify trait(s) needingimprovement

Identify naturally occurringvariability in same/other

s p e c i e s

Select, mutagenize, or trans-form using rDNA methods

Evaluate strains in laboratory,greenhouse or field cages

* fitness, efficacy, stability,mode of inheritance

Conduct small plot trials* efficacy, fitness* mass-rearing* release, sampling& evaluation

Releaseauthorization ?

A--'

Conduct large plot trials* efficacy, persistence, dispersal,

s a f e t y

Implementation, adaptation, education,documentation, cost-benefit analyses

Figure 1. Components of a genetic improvement project with arthropod natural enemies. Dashed linesindicate considerations if recombinant DNA methods are used as the method of genetic manipulation.

What are some of the constraints toinitiating a genetic improvement projectof arthropod natural enemies? First, thefactors limiting the efficacy of the nat-ural enemy must be identified (Figure1). This means that a great deal mustbe known about the biology, ecology,and behavior of the natural enemy. Thisfirst step is extremely crucial, since im-proper identification of the trait needingimprovement could lead to an expensiveand time-consuming project of little

practical value. Second, genetic vari-ability must be available upon which onecan select if using artificial selection. Ifsuch variability does not occur in naturalpopulations, it must be provided forthrough mutagenesis or, perhaps,through recombinant DNA methods.Third, the "improved" natural enemymust be documented to be effective inthe field. Finally, one must assume thatthe cost of the project will be justifiedby the benefits achieved.


Headley and Hoy (1986) recently re-viewed the benefits and costs of an in-tegrated mite management program inCalifornia almond orchards that in-volves the use of a genetically manipu-lated predatory mite. Metaseiulusoccidentalis (Nesbitt) is an effective pre-dator of spider mites in deciduous or-chards and vineyards in western NorthAmerica (Hoy, 1985b). It acquired re-sistance to organophosphorus insecti-cides (OPs) through natural selection inapple orchards in Washington and thisresistance allowed the predator to sur-vive in orchards even though an OP in-secticide (azinphosmethyl or Guthion)was applied to control codling moth(Hoyt, 1969). In 1977, a genetic im-provement project with M. occidentaliswas initiated, with the goal of developingadditional pesticide resistances in thispredator in order to increase its useful-ness in orchard and vineyard pest man-agement programs.

Selection for resistance to carbaryland permethrin was successful, andmulti-resistant strains of M. occidentaliswere obtained through laboratorycrosses and additional selections. Thelaboratory-selected strains were thentested in small plot trials for two years,to determine whether they could becomeestablished in orchards or vineyards,survive the relevant pesticide applica-tions in the field, spread, multiply, ov-erwinter, and control the spider mites(Hoy, 1985b). The small plot trials werethen followed by three years of researchto learn how to implement the predatorsin an integrated mite management pro-gram in almonds (Hoy, 1985b; Headley

and Hoy, 1986). Implementation in-volved developing mass rearing meth-ods, monitoring methods, and learninghow to use reduced rates and numbersof applications of insecticides and acar-icides selective to this predator. The eco-nomic analysis suggested that almondgrowers who adopted the programwould save $60 to $110/hectare. Theprogramatic benefit/cost analysis sug-gested that the return on the researchinvestment will range from 280 to 370percent per year, depending upon thelevel of adoption by almond growers onthe 158,000 hectares of almonds grownin California. This high rate of return

on research investment was attributed,in part, to the fact that more than halfof the research resources were allocatedto field testing and implementation re-search (Headley and Hoy, 1986). Thus,genetic improvement with M. occiden-talis has been shown to be efficaciousand cost effective.

Genetic improvement projects withseveral phytoseiid species have includedselection for enhanced fecundity, tem-perature tolerance, and non-diapause aswell as pesticide resistances (Hoy, 1985c,Table 1). Selection projects are currentlybeing conducted in the U.S.A., China,New Zealand, and France and field trialsare being conducted with some of theselected strains. The successful imple-mentation and economic analyses ofcosts and benefits of these geneticallymanipulated predatory mites will pro-vide impetus to this tactic in biologicalcontrol.

Genetic improvement projects withnatural enemies of insects have been con-ducted for improved climatic tolerances,improved host finding ability, changesin host preference, improved synchro-nization with the host, insecticide re-sistance, non-diapause, and induction ofthelytokous reproduction (Table 2), butto date none of these genetically manip-ulated natural enemies has been used inthe field. Several current projects alsoare in progress and planned field trialswill determine whether use of geneticallymanipulated insect natural enemies canbe implemented in agricultural ecosys-tems. Aphytis melinus, a parasite of the

California red scale, has been selectedfor resistance to carbaryl and the resist-ance level achieved appears to be suffi-ciently high that field trials are justifiedto evaluate this strain's efficacy in Cal-ifornia citrus orchards (Rosenheim andHoy, 1988). The walnut aphid parasite,Trioxys pallidus, has been selected forresistance to azinphosmethyl, and thisstrain was tested in California walnutorchards during the 1988 growing sea-son (Hoy and Cave, 1988). If A. melinusand T. pallidus are able to establish, sur-vive, parasitize their hosts, and success-fully overwinter, then geneticimprovement may be documented to beeffective with insect parasitoids as wellas with predatory mites. ^

The potential for using rDNA tech-nology in genetic manipulation of nat-ural enemies of arthropods has beenreviewed by Beckendorf and Hoy(1985). This new technology offers thepossibility that genetic manipulationcould become more efficient and morecreative; beneficial genes isolated fromone species could be transferred to manyif efficient transformation systems canbe found. This research has a number ofsteps; desirable genes must be identified,cloned, inserted into natural enemies, beincorporated into their genome, be sta-ble, be expressed in the appropriate tis-sues and at the appropriate time, and betransmitted to the progeny. The trans-formed natural enemy strain must thenbe fit and able to perform well in agri-cultural systems (Figure 1). Issues re-lating to the safety of releasing rDNA-

Table 1. Genetic improvement of predatory mites (Acari: Phytoseiidae) through laboratory selection

Trait Species References

Fecundity

Non-diapause

Pesticide resistance

Temperature tolerance

Phytoseiulus persimilis

Metaseiulus occidentalis

Amblyseius fallacisAmblyseius nicholsi

Metaseiulus occidentalis


Typhlodromus pyri


Voroshilov & Kolmakova, 1977

Hoy, 1984, Field & Hoy, 1986

Stockier & Croft, 1982Huang et al., 1987Hoy & Knop, 1981,Roush & Hoy, 1981, Hoy, 1984

Schulten & van de Klashorst,1974, Avella et al., 1985Markwick, 1986

Voroshilov, 1979


Table 2. Attributes of insect natural enemies that have been selected in the laboratory

Trait Species References

Host finding

Host preference

Host synchronyImproved climatic tolerance

Increased fecundity

Insecticide resistance

NondiapauseThelytoky

Trichogramma minutum

Horogenes molestaeParatheresia claripalpisCotesia melanoscelaDahlbominus fuscipennisAphytis lingnanensisTrichogramma fasciatumDahlbominus fulginosusDahlbominus fuscipennisMacrocentrus ancylivorusBracon mellitorAphytis melinus

Trioxys pallidusChrysoperla carneaAphidoletes aphidimyzaMuscidifurax raptor

Urquijo, 1946Landaluz, 1950Allen, 1954Box, 1956Weseloh, 1986Wilkes, 1942White et al., 1970Ram & Sharma, 1977Szmidt, 1972Wilkes, 1942Pielou & Glasser, 1952Adams & Cross, 1967Abdelrahman, 1973Rosenheim & Hoy, in pressHoy & Cave, 1988Grafton-Cardwell & Hoy, 1986Gilkeson & Hill, 1986Legner, 1987

manipulated arthropod natural enemiesremain to be resolved. Safety questionswill probably focus on three issues: 1)whether the transformed strain is stable,2) whether the improved strain retainsits host/prey specificity, and 3) whetherthe ecological range of the transformedstrain has been altered. It will be im-portant to remember that genetic im-provement of arthropod natural enemiesof insect and weed pests will be initiatedbecause there is a serious pest problem.Risks and benefits of such genetic ma-nipulation projects should be evaluatedin terms of the costs and benefits of notdoing the project.

Conclusions

In practice, effective biological con-trol may require that several tactics becombined to achieve effective pest man-agement. Thus, once an exotic naturalenemy is established, specific efforts maybe needed to conserve it. Alternatively,it may have to be released augmenta-tively if it is unable to persist in sufficientnumbers, perhaps because it lacks a dia-pause or alternative hosts. Classical,augmentation, and conservation tacticsshould not be considered to be mutuallyexclusive. Arthropods have been pestsin agriculture for more than 10,000years; it is likely that they will remainserious pests of agriculture, even as itchanges and evolves. New technologiesshould be examined to determine

whether they can result in improved bi-ological control.

Biological control is not being fullyexploited as a method for the control ofpest arthropods in forests, range lands,and agriculture (HufFaker, 1971; Tauberet al., 1985). Additional and continuingefforts should be made in the traditionalclassical, augmentation, and conserva-tion approaches to biological control be-cause the benefits associated with theseapproaches are already known to be sub-stantial and can probably be improved.In addition, research efforts should becontinued to combine and develop newand innovative approaches to biologicalcontrol, including the genetic manipu-lation of natural enemies, the manipu-lation of natural enemy behaviorthrough semiochemicals, and the devel-opment of improved artificial diets andimproved rearing methods so that massproduction for augmentative releases be-comes economical. As summarized byTauber et al. (1985), research needs inbiological control "...form a continuumfrom the very basic to the applied..."

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Low-input farming asset for21st century

"Our inability to accuratelydiet future trends [for agriculture]suggests the need for system resil-iency," Virginia Polytechnic Profes-sor Daniel Taylor told 500 naturalresource professionals meeting inWashington, DC, to assess resourcetrends for the 21st century. Taylorsaid that conventional agriculture,which is characterized by monocul-ture, chemical dependence, hightechnology, and concentrated own-ership, needs to evolve into a systemwith more "flexibility and robust-ness." That means more integrationof animal agriculture with croppingand a decrease of chemical depen-dency, he said.

Pesticide use in the U.S. rose rap-idly from 150 million pounds peryear in 1964 to 500 million poundsin 1982, but "we expect to see thatuse level off and then decline," Tay-lor predicted. Fertilizer use has al-ready peaked and is declining, hereported, with water quality issuesa major factor in the change.

"As economist Kenneth Bouldingsaid, 'while we have to be preparedto be surprised by the future, we donot have to be dumbfounded,"' Tay-lor concluded. He recommendedthat the 1990 Farm Bill be used tohelp create more resilient farmingsystems. The remarks came as partof a three-day conference, "NaturalResources for the 21st Century,"sponsored by the American For-estry Association in mid-November,1988.


biological control of arthropod pests: traditional and emerging technologies

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