Biologically Based Technologies for Pest Control

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Biologically Based Technologies for Pest Control September 1995 OTA-ENV-636 GPO stock #052-003-01449-1

Transcript of Biologically Based Technologies for Pest Control

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Biologically Based Technologies for PestControl

September 1995

OTA-ENV-636

GPO stock #052-003-01449-1

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Recommended Citation: U.S. Congress, Office of Technology Assessment,Biologically Based Technologies for Pest Control, OTA-ENV-636 (Washington,DC: U.S. Government Printing Office, September 1995).

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Foreword

he way the nation manages pests is changing because of efforts to reduce the reliance onconventional pesticides. Driving this change is strong public opinion coupled with actionby Congress and by federal and state agencies. At the same time, pest control needs arerising. Many important pests are now resistant to formerly effective chemical controls.

And new pests continue to enter the country or spread to new locations where they threaten agricul-ture, native ecosystems, or human health.

The farmers, foresters, ranchers, and others who seek to prevent excessive pest damage areincreasingly aware of the shortcomings of conventional pest control approaches. Their need formore pest control options is acute. Current hopes are that integrated pest management (IPM)—which uses alternative tools as well as pesticides—will provide the key to meeting this need whilereducing the reliance on conventional pesticides. This assessment examines an array of the biolog-ically based tools that underpin effective IPM.

The report covers technologies ranging from enhanced biological control of pests by their natu-ral predators and parasites to commercial formulations of microbial pesticides. Today, suchapproaches have joined the mainstream. Biologically based technologies have penetrated mostmajor applications of pest control and are the methods of choice for such widespread pests as thegypsy moth. They could be used more widely to help solve the nation’s pressing need for pest con-trol tools. What happens next will depend largely on federal policies and programs.

The federal government’s role here is extensive through its involvement in research, technologytransfer, plant protection, land management, and pesticide regulation. Annual expenditures forresearch and implementation of biologically based technologies for pest control exceed $200 mil-lion. But the system does not work as well as it might. A better match between national prioritiesand the portfolio of federally supported research would improve delivery of new pest control toolsinto the field. An improved regulatory system would streamline the regulatory process while moreclosely evaluating the occasional high risks. Finally, the relative roles of the private and public sec-tors warrant rethinking, because the private sector on its own will go only so far in supplying newbiologically based tools.

Biologically Based Technologies for Pest Control was requested by three congressional com-mittees: the House Committee on Agriculture; the House Merchant Marine and Fisheries Commit-tee; and the House Committee on Natural Resources, Subcommittee on National Parks, Forests,and Public Lands.

We gratefully acknowledge the contributions of the Advisory Panel, authors of commissionedpapers, workshop participants, and the many additional people who reviewed material for thereport or provided valuable guidance. Their generous, timely, and in-depth assistance made thisstudy possible. As with all OTA studies, the content of this report is the sole responsibility of OTA.

ROGER C. HERDMANDirector

T

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Advisory Panel

Katherine Reichelderfer Smith, Panel Chair

Director, Policy Studies Program

Henry A. Wallace Institute for Alternative Agriculture

Greenbelt, MD

Paul A. BackmanProfessor and DirectorBiological Control InstituteDepartment of Plant PathologyAuburn UniversityAuburn, AL

Ring T. CardéProfessorDepartment of EntomologyUniversity of MassachusettsAmherst, MA

Willard A. DickersonPlant Pest AdministratorNorth Carolina Department of

AgricultureRaleigh, NC

Roger C. FunkVice President of Human and

Technical ResourcesThe Davey Tree Expert

CompanyKent, OH

Harry J. GriffithsChairmanEntomological Services Inc.Corona, CA

Judith A. HansenSuperintendentCape May County Mosquito

Extermination CommissionCape May, NJ

Dennis L. IsaacsonProgram DirectorNoxious Weed Control SectionOregon Department of

AgricultureSalem, OR

Deborah B. JensenVice President, Conservation

Science and StewardshipThe Nature ConservancyArlington, VA

Tobi L. JonesSpecial Assistant to the

DirectorDepartment of Pesticide

RegulationCalifornia Environmental

Protection AgencySacramento, CA

Peter M. KareivaProfessorDepartment of ZoologyUniversity of WashingtonSeattle, WA

Allen E. KnutsonAssociate Professor and

Extension EntomologistTexas Agricultural Extension

ServiceTexas A&M UniversityCollege Station, TX

James B. KramerFamily FarmerHugoton, KS

David W. MillerVice President for Research

and DevelopmentEcoScience CorporationNorthborough, MA

Timothy L. NanceCrop ConsultantGro Technics ConsultingNaples, FL

David O. TeBeestProfessorDepartment of Plant PathologyUniversity of ArkansasFayetteville, AR

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Jeffrey K. WaageDirectorInternational Institute of

Biological ControlAscot, Berks, UK

Michael E. WetzsteinProfessorDepartment of Agricultural and

Applied EconomicsUniversity of GeorgiaAthens, GA

David M. WhitacreVice President, DevelopmentSandoz Agro, Inc.Des Plaines, IL

EXECUTIVE BRANCH LIAISONS

Gary H. JohnstonNational Park ServiceU.S. Department of the InteriorWashington, DC

James Krysan1

Agricultural Research ServiceU.S. Department of

AgricultureWashington, DC

Anne E. LindsayOffice of Pesticide ProgramsU.S. Environmental Protection

AgencyWashington, DC

Thomas C. Roberts2

Bureau of Land ManagementU.S. Department of the InteriorWashington, DC

1 Until February 1995.2 From April 1995.

Sally J. RockeyCooperative State Research,

Education, and Extension Service

U.S. Department of Agriculture

Washington, DC

Judith St. John3

Agricultural Research ServiceU.S. Department of

AgricultureWashington, DC

William S. WallaceAnimal and Plant Health

Inspection ServiceU.S. Department of

AgricultureWashington, DC

Lewis H. Waters4

Bureau of Land ManagementU.S. Department of the InteriorWashington, DC

3 From June 1995.4 Until March 1995.

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Project Staff

Clyde BehneyAssistant Director

Walter E. Parham1

Program DirectorFood and Renwable Reources

Robert Niblock2

Program DirectorEnvironment Program

1 Through February 1994.2 From March 1994.

Elizabeth A. ChorneskyProject Director and Senior

Analyst

Cynthia M. Palmer3

Analyst

John LongbrakeResearch Analyst

Christine Taverna4

Research Assistant

CONTRACTORS AND OTHER CONTRIBUTORS

John M. HoughtonContractor & Workshop

Organizer

Priscilla S. TaylorEditor

Gary Jahn5

Analyst

William Westermeyer6

Senior Analyst

3 From January 1995.4 From May 1995.5 April through July 1994.6 February through May 1995.

ADMINISTRATIVE STAFF

N. Ellis Lewis1

Office Administrator

Kathleen Beil2

Office Administrator

Nellie M. HammondAdministrative Secretary

Kimberly Holmlund2

Administrative Secretary

Sharon Knarvik2

Administrative Secretary

Babette Polzer4

Contractor

Carolyn M. Swann1

PC Specialist

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Contents

1 Summary 1Context and Scope1Current Use and Future Potential of BBTs2Issues and Options3Rethinking Public and Private Sector Responsibilities 6

2 The Context 9An Introduction to Pest Management10Forces Shaping the Future of U.S. Pest Management16Responses by Congress and the Executive Branch23Defining the Terms of OTA’s Assessment25

3 The Technologies 31Evaluating the Technologies31Current Use of BBTs in the U.S.40Obstacles to Expanded Use of BBTs58Improving the Odds of Future Success62Appendix 3-A: Internet Sites for Information on

Biologically Based Pest Control64

4 Risks and Regulations 69Risks from BBTs 69Addressing the Risks 83Regulating the Risks from BBTs: Issues and Options102

5 From Research to Implementation 109Overview 109Educating Users 131From Research to Implementation: Issues and

Options 137

6 Commercial Considerations 145Structure of the BBT Industry146View from the Conventional Pesticide Industry155Issues and Options160

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Appendix A: List of Boxes, Figures, and Tables 167

Appendix B: List of Acronyms 169

Appendix C: Background Reports, Workshops, and Workshop Participants 171

Appendix D: Reviewers 175

References 181

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1Summary

CONTEXT AND SCOPEest management in the United States ischanging. Increasingly, the emphasis ison reducing the reliance on conventionalpesticides.1 Several factors make such

change almost inevitable. Increased rigor of pes-ticide screening, economic forces within the pes-ticide industry, and continuing widespread publicconcern about the harmful effects of pesticidesare contributing to reductions in the number ofavailable pesticides and their allowed uses. Atthe same time, pest control needs are risingbecause of the increasing occurrence of pesticideresistance and newly emerging pest threats. Thegrowing disparity between the available pesti-cides and the number of pests requiring controlwill generate needs for more and a greater vari-ety of pest control tools and techniques.

This problem’s significance has not been loston national policymakers. Both Congress and theexecutive branch have responded in recent years

1 Conventional pesticides are chemical compounds in wide use that kill pests quickly. These chemicals currently pervade all aspects ofpest management in the United States and support annual sales exceeding $8.4 billion.

with initiatives related to providing pest manage-ment tools and expanding the implementation ofintegrated pest management (IPM).2 It is in thiscontext that Congress has asked the Office ofTechnology Assessment (OTA) to examine thecurrent and potential future role of biologicallybased technologies for pest control (BBTs).These technologies are grounded in an under-standing of pest biology and have a relativelylow probability of harmful effects on humanhealth or the environment.3

The assessment covers the following fivetechnologies:

■ Biological Control—Suppression of pest pop-ulations by natural enemies (predators, para-sites, competitors, diseases). Humans canexploit biological control by permanentlyestablishing new natural enemies in a region(classical biological control), by repeatedlyreleasing natural enemies to temporarily boosttheir abundance (augmentative biological con-

2 The term integrated pest management or IPM refers generally to pest management practices that seek to integrate all available tools forpest control—biological, chemical, cultural, and otherwise. See box 2-1 for more detailed discussion of IPM concepts and origins.

3 Biologically based technologies are not, however, risk free. See text that follows and chapter 4 of the report for more detailed treatmentof the potential risk issues.

P

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trol), and by engaging in practices thatenhance the survival and impacts of naturalenemies, e.g., reducing pesticide use (conser-vation of natural enemies).

■ Microbial Pesticides—Relatively stable for-mulations of microorganisms4 that suppresspests by producing poisons, causing diseases,preventing establishment of other microorgan-isms, or other mechanisms. Microbial pesti-cides are designed for large-scale productionand application. The most common one in usetoday is Bt, formulated from the bacteriumBacillus thuringiensis.

■ Pest Behavior-Modifying Chemicals—Exploi-tation of the chemical cues used by livingorganisms to evoke specific behaviors fromother organisms. Pheromones, chemicals thatcommunicate information between membersof a single species, currently are used to dis-rupt pest mating or to attract pests to pesti-cides.

■ Genetic Manipulation of Pest Populations—Release into the pest population of individualsgenetically altered to carry genes that interferewith the pest’s reproduction or impact. Themethod in significant use today is release ofsterile males in order to reduce pest reproduc-tion.

■ Plant Immunization—Enhancement of plantresistance to pests by means other than breed-ing or genetic engineering. Scientists canenhance disease resistance in some plants byexposing them to certain microbes or chemi-cals. Research is also under way to transfercertain predator- and disease-deterring fungiinto plants.

4 Organisms too small to be seen by the naked eye, e.g., viruses, bacteria, fungi, protozoans, and certain nematodes (worm-like animals).

These technologies represent an importantsegment of the alternatives to conventional pesti-cides. Federal expenditures on BBT research andimplementation exceed $200 million annually.BBTs are a major part of the U.S. Department ofAgriculture’s (USDA) emphasis in pest control.BBTs also comprise a significant part of the“reduced-risk pesticides,” “biopesticides,” and“biorational pesticides” that are receiving a gooddeal of attention from the U.S. EnvironmentalProtection Agency (EPA) and state agencies.5,6

CURRENT USE AND FUTURE POTENTIAL OF BBTSEven though conventional pesticides dominateU.S. pest management practices, BBTs have pen-etrated most major applications and joined themainstream. For example, at least 28 statedepartments of agriculture operate their own bio-logical control programs. The USDA Animal andPlant Health Inspection Service (APHIS) as amatter of policy promotes biological controlwhere possible in its programs. For control ofgypsy moth, a major forest defoliator found inmore than 11 states, the U.S. Forest Servicerelies primarily on a combination of microbialpesticides and natural enemies. Numerous farm-ers adjust pesticide selection or spray schedulesin order to minimize harmful impacts on pests’natural enemies. Several major food processingcompanies, such as the Campbell Soup and Ger-ber Companies, have set low tolerances for resi-dues of conventional pesticides in their productsand are promoting “biointensive” IPM amongfarmers who supply their produce.7 And a grow-ing array of microbial pesticides is now available

5 “Reduced-risk,” “biopesticide,” and “biorational pesticide” have all been used with differing meanings, depending on the source, toencompass various combinations of microbial pesticides, botanical pesticides, chemicals that modify pest behavior or growth, augmentativereleases of natural enemies, and conventional pesticides that have new chemistries. OTA will not use these terms because of their ambiguousmeanings.

6 Microbial pesticides and pheromone-based products made up 45 percent of all new pesticide active ingredients registered by EPA in1994.

7 “Biointensive” IPM refers to an IPM system that minimizes pesticide inputs and that uses BBTs for pest control in addition to other cropmanagement practices.

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Chapter 1 Summary 3

Tiny Trichogramma wasps, about the size of the head of a pin,are one of the most widely sold natural enemies for control ofagricultural pests. The wasp shown here iS laying its egg in thelarger egg of a corn earworm (Helicoverpa zea).

J. Clark, University of California Statewide IPM Project

to homeowners for control of landscape andhousehold pests.

Current use of BBTs in the United States ispatchy, however. The major share of BBT usagetargets insect pests of arable agriculture, forestry,and aquatic environments. Use is growing forinsect control in urban and suburban settings asnew microbial and pheromone bait productsbecome available for turf and household pests. Inarable agriculture, BBTs have virtually no role atpresent for weed control; in contrast, classicalbiological control has been used to suppress anumber of weeds of rangelands, pastures, andwaterways. Few BBTs are yet available for con-trol of plant pathogens, although a number ofmicrobial products have been introduced in thepast year for seed treatments and other applica-tions.

Adoption of BBTs has occurred most fre-quently where conventional pesticides are: 1)unavailable because of pest resistance or smallmarket size; 2) unacceptable, such as in environ-mentally sensitive habitats or where human con-tact is high; or 3) economically infeasiblebecause the costs of pesticide use are high rela-tive to the economic value of the resource, suchas in rangeland management. In these situations

the chief advantages of BBTs become significantassets—namely that they reduce reliance on con-ventional pesticides, are relatively benign interms of impacts on human health and the envi-ronment, and, in the case of classical biologicalcontrol, provide lasting, widespread, and low-cost suppression of individual pests.

Adoption is less common where effective andacceptable conventional pesticides exist andwhere numerous pests require simultaneous con-trol. This is largely because BBTs do not usuallycompare favorably when measured against theperformance standards set by conventional pesti-cides. Most have a narrower target range, actmore slowly, provide a less efficient level of pestsuppression, and, if sold commercially, haveshorter field persistence and briefer shelf life. Abiologically based method usually must be inte-grated with other control methods in order toprovide an overall package of pest suppression.Reliance on BBTs thus requires a knowledgeableuser and greater planning.

The limited availability of BBTs also contri-butes to their uneven adoption. At present, consid-erably more effort is focused on BBT researchthan on adaptation of the research findings tofield use. BBTs are presently unavailable formany pest problems due to a lack of the neces-sary research on applications, development, orproduction and delivery technologies. Evenwhen available, certain BBTs remain inaccessi-ble to many end-users who lack sufficient train-ing or appropriate sources of information.

ISSUES AND OPTIONSToday’s national policies on pest managementand pesticide use reduction depend on the devel-opment of alternatives to conventional pesti-cides. Some underlying assumptions about thecapacity of the public and private sectors to sup-port expansion of BBT use may be overly opti-mistic. The federal government potentially exertsa significant influence on BBT adoption throughits extensive and diverse roles in research, devel-opment, implementation, and regulation. Adjust-ment of federal policies and programs in several

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areas could greatly enhance the effectiveness ofefforts to safely bring BBTs into wider use.

❚ Balancing Risks and RegulationsIn looking ahead to expanded BBT use, it isimportant to ask what risks the technologies willbring. BBTs generally rank favorably from theperspective of public health and environmentalsafety. Many are relatively host specific andimpact primarily the targeted pests. Unlike con-ventional pesticides, most BBTs lack mamma-lian toxicity or pathogenicity. Moreover, thedevelopment of resistance by weed and insectpests appears significantly slower for most BBTsthan for conventional pesticides.

Nevertheless, BBTs are not risk free. Somemay pose certain hazards to human health andthe environment. Some of these potential impactsare better documented than others. Allergic reac-tions to fungal pathogens and to insect eggs,scales, and waste in insectaries are the best-understood human health impacts. To scientistswho study the ecology of natural systems, themost significant concerns relate to the impacts ofbiological control and microbial pesticides onnative species and the functioning of ecosystems.A lack of monitoring for such effects during pastdecades means some of the most likely ecologi-cal effects, such as declines in native insect pop-ulations, have probably gone unnoticed.

The significance of any risk depends on howwell the regulatory structure prevents the highimpacts from occurring. Past regulatory reviewof biological control by APHIS has been incon-sistent—too lax in some cases and too burden-some in others. The EPA has done a better job inits oversight of pheromones and microbial pesti-cides under the Federal Insecticide, Fungicide,and Rodenticide Act,8 although the risks posedby upcoming microbial pesticides—some geneti-cally engineered for enhanced target range andlethality—will pose new challenges for theagency. The Food and Drug Administration(FDA) needs to clarify its regulatory responsibil-

8 Federal Insecticide, Fungicide, and Rodenticide Act (1947), as amended (7 U.S.C.A. 136, et seq.).

ities for certain uses where BBT residues maybecome a component of food products.

Chapter 4 of the report presents optionsrelated to:

■ improving APHIS’s regulatory structure forbiological control;

■ strengthening innovations while retaining bal-ance in EPA’s regulation of microbial pesti-cides and pheromones;

■ anticipating food safety issues and theexpanded role of the FDA that will arise asuses of BBTs on harvested produce and infood preparation areas increase; and

■ reducing the likelihood that pests will developresistance to BBTs, specifically the microbialpesticide Bt.

❚ Improving the Pipeline from Research to ImplementationThe federal government plays a large role in theresearch, development, and implementation ofBBTs. At least 11 federal agencies are involved,most within the USDA. Despite the size of theseefforts, BBTs do not move smoothly fromresearch into on-the-ground solutions to pestproblems.

Adjusting the Research AgendaThe gap between BBT research and its use—referred to by some long-time observers as the“valley of death”—was the single most promi-nent problem identified during the OTA assess-ment. It results, in part, from a lack ofinstitutional coordination at several levels withinand among federal departments. Ad hoc interac-tions among scientists working on BBTs fromvarious government agencies and universitieshave generally been quite good. In contrast,problems frequently arise when cooperationbetween institutions is required. The results haveincluded: a poor match between federally sup-ported research and national priorities; abundantresearch that never makes it into the field; and

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Chapter 1 Summary 5

Educating and Influencing Users

Pheromone dispensers are widely used in California peachorchards to suppress the oriental fruit moth (Grapholita molesta)

by disrupting the pest mating.

J Clark, University of California Statewide IPM Project

national programs to control emerging pestthreats that are beset by delays in the develop-ment of appropriate management tools.

The diffuse decision-making structures withinthe USDA research agencies (the AgriculturalResearch Service and Cooperative StateResearch, Education, and Extension Service)often fail to effectively focus research ontonationally identified needs. For example,although herbicides make up the single largestcategory (57 percent) of pesticide use in theUnited States today, only 15 percent of federalBBT research is directed toward control ofweeds. The scattered portfolio of BBT researchrarely addresses all of the research componentsnecessary to enable the practical uses of a givenBBT. No agency has consistently taken responsi-bility for conducting or funding the essentialresearch to translate the work of scientists onBBTs into practicable applications for farmersand other users.

Few farmers will readily embrace technologiesthat involve unfamiliar procedures and uncertainconsequences. Many BBTs require a significantlevel of information to use properly, and farmersoften lack clear-cut instructions or authoritativesources of advice on how to apply them.

The Cooperative Extension Service is theprincipal governmental provider of direct, hands-on services to growers and historically played akey role in farmers’ pest control decisions. Inmost states, however, extension plays only aminimal role in educating farmers about BBTs;most extension agents have had little if any for-mal exposure to biologically based approaches.Moreover, the Cooperative Extension Service’srole in shaping pest management practices isnow secondary to that of the far more numerousprivate consultants in most regions (crop advi-sors, pest control advisors, and pesticide dealersand applicators). However, like extension agents,many private advisors are not well versed inBBTs or 1PM. Many are associated with conven-tional pesticide manufacturers or suppliers andare thus inclined to recommend chemically basedtechnologies. According to representatives ofmajor pesticide companies that also produceBBTs, even their own sales representatives donot adequately promote Bt or other biologicallybased products.

A number of other factors are thought to indi-rectly influence the pest control decisions ofsome users, although most lack adequate docu-mentation. Produce standards set by USDA andour international trading partners, for example,sometimes require minimal pest damage, andmay provide strong incentives for more frequentpesticide application. Certain production con-tracts and other arrangements with food process-ing companies may direct growers to use specificpest management practices.

Chapter 5 of the report presents specificoptions designed to address the shortcomings ofthe federal research system and the indirect influ-ences of the federal government on the pest con-trol decisions of farmers, These options include:

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■ better coordinating the USDA research agendawith national pest management needs identi-fied by EPA and the land management agen-cies;

■ modifying mechanisms of funding BBTresearch to better ensure the research makes itinto field applications;

■ providing an institutional structure for coordi-nating biological control activities at anational level in order to increase the potentialfor success and decrease the risks;

■ addressing currently unmet research needsrelated to weeds and monitoring of BBTimpacts and effectiveness;

■ maintaining the necessary levels of technicalexpertise in IPM and taxonomy; and

■ improving the flow of BBT information tousers.

❚ Commercial ConsiderationsCertain BBTs lend themselves to commercialproduction—specifically, natural enemies foraugmentative release, microbial pesticides, andpheromone-based traps and mating disrupters.Almost all of the biologically based productssold to date have been for control of insect pests.Over the near term, BBTs are thus unlikely tocapture a significant proportion of the conven-tional pesticide market, only about 29 percent ofwhich is aimed at insect control.

Nevertheless, BBTs represent one of the fast-est growing sectors of the pesticide industry.Biologically based products now comprisearound 2 percent of the U.S. pest control marketand 1 percent of the international market(approximately $120 million and $214 million inannual sales, respectively). The companiesinvolved are diverse, ranging from small owner-operated companies to large multinational corpo-rations. Almost all of the major agrochemicalcompanies, such as Ciba-Geigy, have invested tosome degree in BBTs, mostly microbial pesti-cides, although this involvement is somewhattentative.

In general, these are financially troubled timesfor many of the companies specializing in the

development or marketing of BBT products.Numerous small companies operate at a lowprofit margin, are vulnerable to unstable markets,and have difficulty investing in product discov-ery or formulation and production technologies.An important obstacle to wider use is that BBTsdo not move easily through the extensiveentrenched infrastructure currently in place forthe research, development, and marketing ofconventional pesticides.

According to a workshop of private sectorexperts convened by OTA, in the absence of anychange to federal policies and programs, BBTsare likely to experience slow gains and willremain restricted primarily to high-value crops(e.g., fruits and vegetables) and other nicheareas. Due to economic factors within the agro-chemical industry, future conventional pesticideswill tend to be broad-spectrum chemicals that fitpoorly into IPM.

Congress could alter this scenario, however,by adjusting the many influences the federal gov-ernment presently exerts on the BBT industry.

Options set out in chapter 6 of the reportaddress:

■ fashioning public-private partnerships inresearch;

■ supporting development of voluntary productstandards and the registration of BBTs; and

■ enhancing market opportunities for BBTs.

RETHINKING PUBLIC AND PRIVATE SECTOR RESPONSIBILITIESAs Congress looks ahead to the future of pestmanagement in the United States, two things areclear. First, the status quo cannot continue.Future approaches to pest management willrequire a greater diversity of tools and tech-niques. Over the near term, conventional pesti-cides will continue to play a key role, but thechemicals will need to be used more strategicallyin order to enhance natural control of pests andminimize the potential for pest resistance andother harmful impacts.

Second, adjustment of today’s dominant para-digm based primarily on conventional pesticides

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Chapter 1 Summary 7

will not come easily. Alternative technologies donot exist for certain pest problems. Many ofthose that do exist require a change in the wayfarmers and other users think about pest controland its goals and methods.

In the past, the federal government has shoul-dered a significant part of the research and devel-opment of BBTs. The investment is appropriatebecause the costs of not planning for the futurewill fall on the public at large; for example, inreduced agricultural productivity or degradationof native ecosystems because certain pests areuncontrollable, or in health and environmentalimpacts because more harmful pesticides arekept on the market. Moreover, the private sectorcannot or is unlikely to become involved in cer-tain key areas because no marketable product isinvolved (e.g., classical biological control andconservation of natural enemies).

Consideration of the current division of publicand private responsibilities suggests some reap-portioning is warranted, however. Most new bio-logically based products will address control ofinsect pests, with several other new productscoming on line for plant pathogens. Weeds havebeen largely ignored by both the private and pub-lic sectors. Increased public investment mightensure that technical successes in weed controlremain available to farmers, even if the profitmargin is too low to sustain commercial inter-est .9 Conversely, private sector innovations inthe rearing of natural enemies would be morelikely to occur if markets for these products wereexpanded and stabilized; for example, by con-tracting out production of natural enemies andsterile insects for the federal government’s pestcontrol programs.

The effectiveness of federal efforts to bringBBTs into widespread use could be improved.Better mechanisms are needed to ensure that thefederal government’s annual investment of morethan $135 million into BBT research delivers

Many land managers expect biological control to be an impor-tant part of the solution to widespread pests on low-valuelands—such as this yellow starthistle (Centaurea solstitialis), anoxious weed that IS now spreading across western range-Iands.

J. Asher, Bureau of Land Management

solutions to national priorities. And certain goalsand approaches of Cooperative Extension meritadjustment to ensure the greatest impact of thesystem’s limited resources.

Scientists have been warning for years thatmeeting the nation’s future needs in pest man-agement will require new tools and techniques.While BBTs won’t fulfill all of these needs, theycould play a significant role. Safely bringing bio-logically based tools into the hands of farmersand other users will require certain changes inthe operation of various federal agencies. Thereport that follows focuses on the underlyingtechnical and institutional issues and identifiespotential solutions.

9 A good example is Collego, a very effective microbial pesticide for weed control that became a commercial failure because it could notsustain a large enough market,

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2The

Context

he way pests are managed in the UnitedStates is changing. A growing emphasisis on reducing the reliance on conven-tional pesticides. Strong public opinion

coupled with legislative and executive actions bystate and federal governments is driving thischange. Farmers, foresters, ranchers, homeown-ers, and others who seek to prevent excessivepest damage are increasingly aware of the short-comings of many conventional approaches topest control. Yet their need for effective methodsis acute. Meeting this need with a diversity ofpest control tools and techniques poses a signifi-cant challenge. It is in this context that Congresshas asked the Office of Technology Assessment(OTA) to examine the current and potentialfuture role of biologically based technologies(BBTs) in the nation’s pest management prac-tices.

The OTA assessment covers a group of tech-nologies that are grounded in an understandingof pest biology and generally have the following

characteristics that differentiate them from mostconventional pesticides:1

■ narrow spectrum of action, that is, affectingonly one or a narrowly defined class of organ-isms;

■ relatively low probability of harmful environ-mental impacts; and

■ general lack of significant adverse impacts onhuman health.2

These BBTs for pest management are biologi-cal control, microbial pesticides, pest behavior-modifying chemicals, genetic manipulation ofpest populations, and plant immunization (box2-1). The tools raise a unified set of technical andpolicy issues. BBTs comprise a significant partof the “reduced-risk pesticides,” “biopesticides,”and “biorational pesticides” that are receiving agood deal of attention in federal and state policyinitiatives.3

OTA’s assessment takes a critical look atthese BBTs. This chapter describes past, current,

1 Conventional pesticides are chemical compounds in wide use that kill pests quickly (267).2 The technologies are not, however, risk free. See chapter 4 for a detailed analysis of the major risk issues.3 “Reduced-risk,” “biopesticide,” and “biorational pesticide” have all been used with differing meanings, depending on the source, to

encompass various combinations of microbial pesticides, botanical pesticides, chemicals that modify pest behavior or growth, augmentativereleases of natural enemies, and conventional pesticides having new chemistries. This report does not use these terms because of this ambigu-ity.

T

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and potential future trends in U.S. pest manage-ment. Chapter 3 examines the effectiveness ofBBTs and their future potential. The remainderof the report identifies the many activities of thefederal government that affect the availabilityand use of BBTs (table 2-1). The potential risksof BBTs and how these are addressed throughfederal regulation are covered in chapter 4.Chapter 5 focuses on the public-sector roles inthe research, development, and implementationof BBTs. And chapter 6 looks at BBTs from thevantage of private-sector companies involved inthe production of pest control products.

AN INTRODUCTION TO PEST MANAGEMENTThroughout history, humans have sought to elim-inate or reduce the abundance of living organ-isms that cause problems. The “pests” includeanimals, plants, insects, and microbes4 thatreduce agricultural productivity, damage forestsand gardens, infest human dwellings, spread dis-ease, foul waterways, and have numerous otherdeleterious effects. Left unimpeded, their eco-nomic impacts in the United States wouldamount to billions of dollars annually. The WeedScience Society of America has estimated thatannual U.S. losses to agriculture if weeds were

4 Microbes include viruses, bacteria, and other organisms that are too small to be seen by the human eye. Many microbes that are pestscause animal or plant diseases.

uncontrolled would exceed $19.6 billion—almost five times the costs under current controlregimes (32). The environmental impact of pestscan be equally profound: European gypsy moth(Lymantria dispar) now infests some 255 millionacres in the United States; if the pest was leftuntreated, its annual defoliation of trees couldfundamentally change the composition of hard-wood forests (385).

Although what constitutes a “pest” is highlysubjective, needs for pest control identified byU.S. consumers, agribusiness, and industry nowsupport a multibillion-dollar infrastructure ofpesticide production, pest control companies,and consultants on pest control methods. U.S.expenditures for pesticides exceeded $8.4 billionin 1993, approximately one-third of the worldmarket (table 2-2) (399)

Pest control is quite literally a science of thespecific. In agriculture, each pest and crop com-bination represents a different problem that canfurther vary with the specific location and timeof year. There are literally thousands of (crop ×pest × site) combinations, each differing in itspotential impact and in the way that it is mostsuccessfully and appropriately controlled. Pestsin other environments, such as parks, suburbanlandscapes, and urban dwellings, pose a similarlycomplex array of management needs.

CHAPTER 2 FINDINGS

■ The need for new pest control methods and systems will grow in the future. The number of availableconventional pesticides is declining, especially for minor uses, because of regulatory constraints, eco-

nomic forces, and continuing public concern. At the same time, the number of pests requiring newcontrol methods is increasing as more pests become resistant to pesticides and new pest threats

emerge.■ Congress and the executive branch have sought to address the need for pest control in the future by

pressing to diversify available pest control technologies and to expand the use of integrated pest man-agement. Biologically based technologies underpin many of these efforts. An assessment of these

technologies provides a “bottom-up” view of whether and how effectively the national infrastructure forresearch, development, and implementation can deliver on this agenda.

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Chapter 2 The Context | 11

❚ The Role of Conventional PesticidesConventional pesticides greatly simplify controlof these diverse problems. Most conventionalpesticides are broad spectrum—providing con-trol for numerous pests simultaneously. They arerelatively easy to use, because most chemicalsare applied with similar methods and allow a fairmargin of error in application technique. Perhapsmost important, conventional pesticides areeffective at killing pests and are relatively inex-pensive.

Widespread use of conventional pesticides,however, is a recent development. Prior to the1940s, U.S. farmers relied primarily on non-chemical methods such as crop rotation, tillage,and hand removal to minimize pest impacts

(433). A number of inorganic salts (e.g., coppersulfate, lime sulfur, and lead arsenate) and botan-ically derived compounds (e.g., pyrethroids androtenone) had come into use in the late 1800s andearly 1900s. But chemical pest control did nottruly burgeon until after World War II, with theincreasing availability and use of DDT and otherchlorinated hydrocarbon, organophosphate, andcarbamate pesticides. From the 1950s to the1980s, use of conventional pesticides in theUnited States grew dramatically, doublingbetween 1964 and 1978 (figure 2-1) (399). Theincreased use paralleled a growing mechaniza-tion of farming practices and a drop in the num-ber of people engaged in farming. An example ofhow great the change has been can be seen in the

BOX 2-1: Scope of the OTA Assessment

Pest Control Technologies Within the Scope of the OTA Assessment■ Biological Control: the use of living organisms to control pests (includes predators, parasites, com-

petitors, pathogens,1 and genetic engineering applied to this approach)■ Microbial Pesticides: formulations of live or killed bacteria, viruses, fungi, and other microbes that

are repeatedly applied to suppress pest populations (includes Bt formulated from Bacillus thurin-giensis, nuclear polyhedrosis viruses (NPVs), and genetic engineering applied to this approach)

■ Pest Behavior-Modifying Chemicals: the use of chemicals to trap pests or to suppress pest mating(includes pheromones)

■ Genetic Manipulations of Pest Populations: genetic modification of pests to suppress their repro-duction or impacts (includes releases of sterile insects)

■ Plant Immunization: non-genetic changes to crop or landscape plants that deter insect pests orreduce susceptibility to diseases (includes induced immunity and endophytes)

Pest Control Technologies Outside the Scope of the OTA Assessment■ Chemical Pesticides: chemicals that kill pests (inorganic substances like arsenic-containing salts;

synthetic organic compounds like organophosphates, carbamates, and triazines; insect growthregulators that mimic insect hormones; and synthesized and naturally occurring botanical pesti-

cides)■ Physical, Mechanical, and Cultural Controls: nonchemical pest control by methods such as crop

rotation, tillage, mechanical removal of pests (e.g., by hand or vacuums), and heat treatment■ Plant Breeding and Enhanced Resistance to Pests: development of plant cultivars that are less sus-

ceptible to pest damage either through plant breeding or genetic engineering

1 Pathogens can be used as biological control agents if they are released and then spread on their own. They can also beformulated into microbial pesticides that are applied repeatedly.

NOTE: Box 2-5 at the end of this chapter describes in detail certain subcategories of the technologies outside the scope of thisassessment that are receiving increased attention for the same reasons as BBTs.

SOURCE: Office of Technology Assessment, 1995.

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TABLE 2-1: Roles of Federal Agencies Related to Biologically Based Pest Controland Location of Discussion in This Report

Agency

Regulates production or use of BBTs

Conducts research

Funds outside research

Implements technology in pest control programs

Educates end users

Transfers technology to the

private sector

(Chapter 4) (Chapter 5) (Chapter 5) (Chapter 5) (Chapter 5) (Chapter 6)

USDA Agricultural Research Service (ARS)

X X

USDA Cooperative State Research, Education, and Extension Service (CSREES)a

X X X

USDA Forest Service X X

USDA Animal and Plant Health Inspection Service (APHIS)

X Xb X Xc Xc

U.S. Environmental Protection Agency (EPA)

X X X X

Food and Drug Administration (FDA)

X

Management agencies of the U.S. Department of the Interior (DoI)d

X Xe X

a CSREES is a newly formed agency that incorporates prior functions of the Extension Service and the Cooperative State Research Serviceb APHIS conducts “methods development” research, which translates the findings from more fundamental research into on-the-ground applica-tions.c The National Biological Control Institute produces a variety of public education materials and has provided about $1.5 million in grants for edu-cation and implementation of biological control over the past four years.d The National Park Service, the Bureau of Land Management, the Bureau of Reclamation, and the U.S. Fish and Wildlife Service.e Mostly via “pass-through” funds to the ARS for research on biological control of rangeland and other weeds.

SOURCE: U.S. Congress, Office of Technology Assessment, 1995.

TABLE 2-2: User Expenditures for Pesticides in the U.S. by Sector, 1993

Sector Total in millions $ Percentage

Agriculture 6,130 72.2

Individuals/Communities/Government 1,136 13.4

Home and Garden 1,218 14.4

Total $8,484 100.0%

SOURCE: U.S. Environmental Protection Agency, Pesticide Industry Sales and Usage: 1992 and 1993 Market Estimates, A.L. Aspelin, 733-K-94-001 (Washington, DC: June 1994).

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2,000

0- ‘1965 67 69 71 73 75 77 79 81 83 85 87 89 91 93

SOURCE: U.S. Environmental Protection Agency, Pesticide Industry Sales and Usage: 1992 and 1993 Market Estimates, A.L. Aspelin, 733-K-94-001 (Washington, DC: June 1994).

NOTE: Usage level is reported in millions of pounds of “active ingredient.” The active ingredient is the component of a commercial product that

has pesticidal properties. Newer pesticides tend to have active ingredients that are more potent and can be applied at a lower dosage level.

Consequently, the leveling-off in the 1980s in the figure does not necessarily translate into a stabilization of pesticide use according to numbersof acres treated, numbers of products applied, frequency of pesticide application, or other relevant measures.

figures for cultivation of corn, cotton, and wheat:herbicides were applied to only 10 percent ofacreage in 1952, but climbed to 90 to 95 percentof acreage by 1980 (378).

Conventional pesticides now pervade allaspects of pest management in the United States.More than 900,000 U.S. farms use pesticides(399). In 1993, pesticides were applied to morethan 80 percent of the acreage planted in corn,cotton, soybeans, and potatoes (377). Between35,000 and 40,000 commercial pest control com-panies and 351,600 certified commercial applica-tors apply pesticides to building, home, andlandscape pests (399). Each year such commer-cial operations treat an estimated 20 percent ofthe 6.1 million U.S. households for indoor pestssuch as cockroaches (424). Most of these homes(85 percent) also contain pesticidal products, themajority of which (70 percent) had been usedwithin the past year, according to the 1990

National Home and Garden Pesticide Use Surveycommissioned by the Environmental ProtectionAgency (EPA) (424).5

❚ The Spectrum of Approaches toPest Control in Practice TodayToday, the extent to which people seeking tocontrol pests rely on conventional pesticides var-ies (figure 2-2). Some depend on a number ofother pest control tools as well, including culturalpractices, use of pest-resistant crop cultivars, andthe BBTs that are the subject of this assessment.

At one end of the spectrum are those who useonly conventional pesticides, often applyingthem as a prophylactic measure according tosome regular, predetermined spray schedule. Atthe other end are those who control pests by acombination of numerous non-chemical tools,and use conventional pesticides either as the lastmethod of choice or not at all.

5 A total of 2,078 households in 29 states were surveyed, with results statistically extrapolated to a target population of 84,573 house-

holds.

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14 Biologically Based Technologies for Pest Control

Use of conventional pesticides

Methods referred to as Integrated pest management (1PM) In various contexts

SOURCE: Office of Technology Assessment, 1995,

The gradation from one end of the spectrum tothe other entails increased targeting of pesticideapplication and incorporation of a greater num-ber of pest control tools and techniques. Diversi-fication of pest control approaches beyond theregularly scheduled use of conventional pesti-cides requires planning as well as a greaterunderstanding of pest biology and ecology andthe specific effects of each control technology.This thoughtful incorporation of various controlmethods into an overall pest suppression plan hasgenerally been referred to as integrated pest man-agement (IPM)6 (box 2-2). Note that a diverse

range of approaches have all been referred to as1PM by various sources (figure 2-2).

Most users currently fall toward the left andcenter of figure 2-2. For example, according to a1993 survey of pest control professionals com-missioned by Sandoz Agro and conducted by theGallup Organization? only 32 percent reportedhaving ever used 1PM, with rates being highestamong pest control operators (85 percent) andlowest among farmers (19 percent) (302).7 Amore precise survey by the Economic ResearchService of the U.S. Department of Agriculture(USDA) showed that acreage under 1PM varied

6 The term IPM has been used with a good deal more precision in the scientific and technical literature on pest management, although var-

ious authors use it to mean different things, For a thoughtful analysis of how 1PM concepts and definitions have evolved since the 1950s, seeref. 44.

7 Survey was of 2,361 professional lawn care operators, golf course managers, pest control operators, mosquito district managers, road-

side vegetation managers, small-animal veterinarians, and farmers, Note that the meaning of 1PM was not specified in the survey. Resultsthus indicate respondents’ perceptions of whether they have ever used IPM, Some using varied techniques or monitoring pest levels may notrefer to their management practices as 1PM.

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BOX 2-2: What Is Integrated Pest Management?

The concept of integrated pest management (IPM) originated in the late 1950s and 1960s, when ento-mologists at the University of California began to detect failures of pest control as a result of overuse ofinsecticides. Some pests became difficult to control because they developed resistance to formerlyeffective chemicals. And populations of certain other insects that had previously not been consideredpests surged to outbreak levels. These “secondary pest outbreaks” were attributed to the harmful effectsof pesticides on natural enemies—the insect predators and parasites that occurred naturally in fields andotherwise kept secondary pests in check through biological control.

IPM developed as a way to avoid the problems of insecticide resistance and secondary pest out-breaks by integrating biological and chemical control. Its cornerstones were:

■ “Natural” control should be maximized, enhanced, and relied on whenever possible. Natural controlresults from factors both within (i.e., biological control) and outside (i.e., weather) human influence;

■ Pesticides should be used only when the abundance of a pest reaches a threshold level thatcauses economically significant damage. Such restraint minimizes the harmful effects of pesticides

on natural enemies.

Since the 1960s, ideas about IPM have expanded and changed. Additional pest management toolshave come into wider use, and IPM concepts have been applied to other types of pests with a resulting

proliferation of related terms like “integrated weed management” and “integrated disease management.”

Practitioners now often use IPM to refer more generally to an approach that integrates all availabletools for pest control—biological, chemical, cultural, and others. The idea that chemicals should be

applied only when a pest is detected at an (economically or aesthetically) significant level of abundancehas been retained. What is lost in many current applications, however, is the concept that biological con-

trol should form one of the foundations of IPM. One consequence, according to some critics, is that IPMas practiced today too often becomes integrated pesticide management instead.

Right now the difference between these interpretations of IPM may make very little difference in prac-tice. Many users would be hard pressed to base a pest control system on natural control because they

have access to little of the necessary information and relatively few alternatives to conventional pesti-cides.

The distinction does, however, make a great deal of difference in another regard. The two interpreta-

tions lead to very different conclusions regarding the types of research that must underpin IPM. A corereliance on natural control requires emphasizing research into the ecology of pest systems. It also

requires giving greater weight to pest control methods that are compatible with biological control.

SOURCES: Office of Technology Assessment, 1995, and J.R. Cate and M.K. Hinckle, Integrated Pest Management: The Path of aParadigm, National Audubon Society (Alexandria, VA: Weldon Printing Inc., July 1994).

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with type of crop and pest, but that an absence ofpesticide use is rare (table 2-3) (377).

FORCES SHAPING THE FUTURE OF U.S. PEST MANAGEMENTBecause conventional pesticides are easy to useand effective, they are the sole or primary toolused by most practitioners today to control thenumber and impact of pests. But constraints arebeing imposed on the nation’s pest managementpractices. Some—such as the increased rigor ofpesticide screening prior to registration, eco-nomic forces within the industry, and continuingwidespread public concern—will tend to limitgrowth in the number of available pesticides(especially insecticides and fungicides) and theiruse. At the same time, increasing resistance topesticides and newly emerging pest threats willcause the need for pest control to rise. The result-

ing gap between pests requiring control andavailable pesticides will generate the need formore and a greater variety of pest control toolsand techniques—essentially a centerward shift ofthose toward the left end of the spectrum in fig-ure 2-2.

That such needs already exist is evident fromEPA data on exemptions under section 18 of theFederal Insecticide, Fungicide, and RodenticideAct (FIFRA), the authorizing statute under whichEPA regulates registration and use of pesticides.8

These exemptions are granted under emergencycircumstances to allow use of a pesticide withoutthe normal registration requirements that ensuresafety to human health and the environment.According to EPA, at least 200 exemptions arebeing approved each year (164,19). Resistance topesticides, cancellation of a pesticide previouslyin use, and emergence of new pests are the most

8 Such exemptions are authorized under section 18 of FIFRA (1947) as amended (7 U.S.C.A. 136, et seq.) (105).

TABLE 2-3: Use of Integrated Pest Management on U.S. Crops

Do not use IPM

Monitor levels of pests and use pesticideswhen levels exceed set thresholds,

but use no additional pest control tactics

Use additional pest control tactics inan IPM program

Do not use pesticides

Percent of acres

Fruits and nuts 42 6 44 8

Vegetables

Insect control 38 9 43 10

Weed control 60 2 33 6

Disease control 29 12 29 30

Corn

Insect control 15 52 22 11

Weed control 45 2 51 2

Soybean

Weed control 39 2 57 2

Fall Potatoes

Insect control 25 3 69 3

Weed control 30 1 65 5

Disease control 14 5 58 22

SOURCE: Adapted from U.S. Department of Agriculture, Economic Research Service, Adoption of Integrated Pest Management in U.S. Agricul-ture, prepared by A. Vandeman et al., AIB-707 (Washington, DC: September 1994).NOTE: Survey was conducted during 1991 and 1992 and covered from 70 to 100 percent of total acreage per crop in the United States.

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common reasons for exemptions. The level ofuse of these exempted chemicals is uncertain.Nevertheless, one consequence of the growingbacklog of pest control needs is circumvention ofthe standard criteria that ensure safe pesticideuse.

❚ Regulation of Conventional PesticidesMore rigorous federal regulation of conventionalpesticides is directly and indirectly causing cer-tain pesticides to be withdrawn from U.S. mar-kets. These losses are unlikely to be completelyoffset by the new chemicals coming on line.

Over the past few decades, the Congress hasset a clear national policy, through amendmentsin 1972 and 1988 to FIFRA, to phase out con-ventional pesticides that are harmful to humanhealth or the environment. These amendmentsrequired reevaluation and reregistration of pesti-cides already on the market to bring them intoline with current testing requirements.

A significant number of pesticides areexpected to disappear from U.S. markets as aresult of the reregistration requirements. In theearly 1990s, companies elected not to reregisteran estimated 25,000 of the 45,000 products onthe market (401). The total number that will ulti-mately disappear is unknown, as are the specificreasons why companies decide not to reregistereach product. According to EPA, 19,000 of thedropped registrations were for older productsthat had not been produced in the three previousyears (401). With respect to the remaining 6,000products, companies may not have sought thereregistration of some that would not meet themore scrupulous registration criteria. But a morecommon reason may be that manufacturers havedetermined that the potential market size for cer-tain products does not justify the costs of reregis-tration.

Experts expect that many pesticides fallinginto the last category are those that serve rela-tively small markets, the “minor use” pesticides,

for use in crops like fruits, vegetables, and nutswhere the potential market size per registration isquite small, especially when compared with mar-kets for major crops like corn, wheat, soy, andcotton. Corn, for example, was grown on about79 million U.S. acres in 1992; in contrast, theacres devoted to all vegetables combinedamounted to only 4.6 million (379). Industryexperts now anticipate that manufacturers willdrop the registrations on 4,000 pesticides cur-rently labeled for only minor uses; about 1,000 ofthese have significant uses (335).

Congress has sought to redress these eco-nomic disincentives for registration of minor usepesticides in a number of ways. The IR-4 pro-gram,9 administered by USDA through theCooperative State Research, Education, andExtension Service (CSREES) and funded at $5.7million in fiscal year 1995, supports the develop-ment of data for minor use registrations. IR-4works in conjunction with the AgriculturalResearch Service (ARS) minor use program,funded at $2.1 million for 1995. A number ofbills have been introduced with strong bipartisansupport in the 103d and 104th Congresses10 toreduce the costs of minor use registrations—most recently in H.R. 1627 introduced May 12,1995.

Removal of the economic constraints will notcompletely counter the effects of reregistrationon the number of available pesticide products.The active ingredients and products that havebeen reregistered first are those that require theleast new data on environmental and health risks.Older chemicals long on the market generallyrequire more data to support reregistration andwill be the last to be reregistered. Far less isknown about the potential risks of these chemi-cals. As the chemicals come under review, addi-tional products may have uses restricted or beremoved from the market due to risk consider-ations, not economic forces.

Costs of pesticide research and developmenthave risen steadily in the recent past. These

9 The Interregional Research Project, No. 4 was begun in 1963 by directors of the State Agricultural Experiment Stations.10 Related bills include H.R. 967 and S. 985 in the 103d Congress and H.R. 1352, H.R. 1627, and S. 794 in the 104th Congress.

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costs, coupled with the more careful scrutiny ofpotential impacts, have slowed the rate at whichnew pesticide products have been marketed(150) (see chapter 6). Moreover, companies areincreasingly seeking to position new products inmajor, not minor markets. The effects of thistrend on the number of pesticides available in theUnited States are uncertain, but the developmentof new pesticides is unlikely to compensate forthe losses of current pesticides through the rereg-istration process, especially of those for minoruse markets.

Development of pesticide replacements mayalso be impeded by the rate of the pesticidereregistration process. EPA has been widely crit-icized for its slow action on reregistration,prompting repeated prodding by Congressthrough oversight hearings (336). The delaysallow continued marketing of older pesticides,potentially creating a deterrent to the develop-ment of new, lower-risk alternatives (190).

❚ Public ConcernAssessment of the benefits and risks of conven-tional pesticides is beyond the scope of thisreport. The use of pesticides in the United Statesover the past several decades has obviously hadconsiderable benefits to agriculture and publichealth, but has also caused harm. The body ofinformation addressing pesticide impacts onhuman health and the environment is complexand large (202). Certainly, humans and wildlifeexposed to certain pesticides under specific con-ditions have shown short- and long-term adverseimpacts ranging from poisoning to sterility andcancer (55,202). The thousands of chemical for-mulations in use today vary greatly in theirmodes of action, toxicological profiles, and othersignificant features. Effects of any given pesti-cide depend not only on such specific character-istics, but also on the ways in which it is used,the environment into which it is released, and the

duration and level of exposure of humans andother living organisms.

Despite this complexity, it is clear that thepublic now has substantial concern about expo-sure to pesticides. This concern is driven as muchby perceptions about how much we don’t knowabout pesticide impacts as by what we do. It iscompounded by the frequent reports of unantici-pated exposure from groundwater contamination,food residues, and improper pesticide use andstorage. The resulting public sentiment can bepowerful, especially if the level of uncertainty isgreat, even in the absence of technical evidencethat an unambiguous risk to public health or theenvironment exists (e.g., box 2-3).

The level of media coverage suggests thatpublic interest is constant and intense. OTA’ssearch of six major newspapers across the coun-try showed that they run, on average, more thanthree related articles a week, providing a constantchronicle of public exposure, health impacts, andunintended contamination of food and the envi-ronment.11 Not surprisingly, the media focus onevents of greatest public interest, such as recentlyreported widespread contamination of tap waterby agricultural herbicides in the Midwest (199)and the potential effects of pesticides on repro-duction in humans and wildlife (323).

Recent surveys consistently show that thepublic is genuinely concerned about pesticideresidues in food (421). For example, a 1990 sur-vey of 1,900 U.S. households by researchersfrom the USDA Economic Research Serviceshowed that the majority were concerned aboutpesticide safety and food residues (206). Morethan half of the respondents expressed the beliefthat foods were unsafe when grown using pesti-cides at approved levels. The majority also didnot believe that the health risks of pesticide useare well understood and agreed that pesticidesshould not be used on food crops because therisks exceed the benefits (206).

11 OTA’s search covered the years 1992, 1993, and 1994 for the following newspapers: New York Times, St. Louis Post-Dispatch, Wash-ington Post, Chicago Tribune, Houston Post, and Los Angeles Times. Search criteria covered various types of pesticides and health or envi-ronmental impacts.

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Chapter 2 The Context | 19

Concern about pesticide food safety issuesgained new impetus in 1993 with the release ofthe National Research Council’s highly publi-cized report on “Pesticides in the Diets of Infantsand Children.” The study concluded that childrenand infants may be uniquely susceptible to thetoxic effects of pesticides and are at greater riskthan adults from some chemicals. Past riskassessments may not always have adequatelyprotected infants and children because they didnot explicitly account for these differing impacts,as well as for differences between adults andchildren in diet and other factors—and hence inpesticide exposure levels (241).

Consumer worries about food safety havefueled a 20 percent annual growth in the marketfor organically grown products since 1989. Salesby U.S. companies amounted to $2.3 billion in

1994 (226). Pest control professionals also reportgrowing public concern. In the 1993 Sandoz sur-vey of pest control professionals, 76 percentreported greater public concern about the envi-ronmental impacts of pest control than five yearspreviously (302). One response to this growingconcern has been a reduction in pesticide use. Ina 15-state survey of 9,754 farmers conducted in1994, 82 percent reported using less or the sameamount of pesticides than five years ago, com-pared with only 6 percent reporting an increasein pesticide use (131).

❚ Pesticide ResistanceAn increasing number of pests—insects, weeds,and plant diseases—have become resistant topesticides that formerly were effective in con-trolling them. Alternative control technologies

BOX 2-3: Alar: A Case Study on the Influence of Public Opinion

In early 1989, the television show 60 Minutes and other media sources focused public attention on areport from the Natural Resources Defense Council (NRDC) charging that children were particularly at

risk from exposure to residues of cancer-causing agents in their food. The NRDC report identified as anexample Alar, a chemical widely used in apple production to enhance fruit color and to keep fruit from

falling off trees. Demand for fresh apples plummeted and concern about the presence of other chemicalresidues on produce increased. Losses to apple growers caused by diminished sales exceeded $100

million that spring.

The NRDC report stated that Alar is a potent carcinogen and that children face particular risk. The sci-

entific information underlying this assertion was inconclusive, however. In 1973, scientists in Omaha,Nebraska, had found evidence that unsymmetrical dimethyl hydrazine (UDMH), a chemical comprising

1 percent of Alar, was carcinogenic to mice at very high doses. EPA declared these results “unscientific”because the mice received excessively high doses of the chemical. Subsequent tests found effects on

mice only at extremely high doses and no effects on rats at any level of exposure. Neither U.S. nor Britishregulators found sufficient justification in the research to ban the use of Alar.

Alar, like other plant growth regulators, is regulated as a pesticide by EPA. The strong public outcry

against Alar following the media coverage forced EPA to reassess its findings. The agency subsequentlydetermined that the risks of Alar were too high and pulled the chemical from the market.

Uncertainty was the real issue underlying the debate about Alar. Because there was no proven risk,

government regulators and industry assumed that the chemical was safe. In contrast, the possibility thatAlar might cause cancer led NRDC and parent groups to call for the chemical’s prohibition—especially in

light of the high consumption of apples and apple products by infants and children and the uncertaintiesregarding long-term effects of exposure to carcinogens early in life.

SOURCES: E. Marshall, “A is for Apple, Alar, and . . . Alarmist?” Science 254(5028):20–4, Oct. 4, 1991; J.D. Rosen, “Much AdoAbout Alar,” Issues in Science and Technology 6:85, Fall 1990; D. Warner, “The Food Industry Takes the Offensive,” Nation’sBusiness 79(7):42–45, July 1991; and F.E. Young, “Weighing Food Safety Risks,” FDA Consumer 23(7):8–14, September 1989.

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may provide the solutions to management ofsome resistant pests. They also will become inte-gral components of strategies to slow the rate atwhich resistance develops (77,111). Abundantevidence exists that the use of multiple tactics tocontrol a pest slows the rate at which the pestdevelops resistance to any single tactic in thearsenal (125).

A pest becomes resistant to a formerly effec-tive pesticide when the chemical ceases to pro-vide adequate control. Resistance developsbecause repeated exposure to the pesticidecauses the selective survival of pest strains thatcan tolerate the chemical. Farmers and otherusers often find themselves applying the pesti-cide at an ever-increasing rate to achieve thesame level of pest control. Eventually, the pesti-cide may cease to have any effect on the pestwhatsoever.

Evidence of pesticide resistance was observedas early as the 1950s. As of 1992, the numbers ofresistant species worldwide were estimated at504 arthropods (including insects and arachnids,such as mites), 87 weeds, and 100 plant patho-gens (68).

As of 1988, at least 18 herbicide-resistantweed species had been reported from 31 states(198). Twelve of these species have shown resis-tance to triazines, the most widely used categoryof herbicides. More than three million acres in

the United States are now infested with resistantweeds (198). They include such well knownweeds as cheatgrass (Bromus tectorum), a com-mon seed contaminant and cause of fire hazardson western rangelands, and black nightshade(Solanum nigrum), a common crop weed whosetoxic berries can contaminate harvests of peasand beans (425).

Today in the United States at least 183 insectand arachnid pests are resistant to one or moreinsecticides; 62 of these have developed resis-tance to synthetic insecticides within at least twoof the three major categories of these productsnow in use (organophosphates, carbamates, pyre-throids) (112). California scientists believe thatalmost every arthropod pest in the state is resis-tant to at least one insecticide, and some popula-tions of such important pests as the tobaccobudworm (Heliothis virescens) in cotton andleafminers in certain vegetable crops (Liriomyzasativae) cannot be effectively controlled by anychemical now available (410). Table 2-4 showsthe most critical cases today of multiple resis-tance among arthropod pests in the United States.George Georghiou, a renowned world expert oninsecticide resistance, predicts that new instancesof pest resistance to specific insecticides willpose a continuing impediment to effective con-trol through conventional pesticides (112).

TABLE 2-4: Critical Cases of Multiple Insecticide Resistance in the U.S. Today

Pest Major impacts Resistant to

OP* C P Oth

Two-spotted spider mite(Tetranychus urticae)

Attacks most greenhouse-grown plants; also damages grapes, vegetables, and field and orchard crops

X X X X

Colorado potato beetle(Leptinotarsa decemlineata)

Attacks potato, tomato, eggplant, tobacco, and other crops; found throughout most of the United States

X X X

Southern house mosquito(Culex quinquefasciatus)

Bites humans and can transfer encephalitis X X X X

House fly(Musca domestica)

Most abundant fly in human dwellings; causes annoyance, spreads filth, and is the suspected vector of numerous human diseases; distributed worldwide

X X X X

Little house fly(Fannia canicularis)

Occasional parasite of the human urinary tract and intestines

X X X

(continued)

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Chapter 2 The Context | 21

Pest Major impacts Resistant to

OP* C P Oth

Sweetpotato whitefly(Bemisia tabaci)

Destructive pest of irrigated cotton and vegetables; has caused annual losses in excess of $100 million to California agriculture during severe outbreaks; damages greenhouse crops

X X X

Silverleaf whitefly(Bemisia argentifolii)

Attacks over 600 plants including melons, squash, tomatoes, lettuce, cotton, and poinsettias; has caused over $500 million in damage in California, Arizona, Florida, and Texas

X X

Greenhouse whitefly(Trialeurodes vaporariorum)

Attacks cucumber, tomato, lettuce, geranium, and many other plants

X X X

Cotton aphid(Aphis gossypii)

Important aphid pest of agriculture, affecting cotton, melons, citrus, and other crops; distributed throughout the United States; most destructive in the South and Southwest

X X X

Pear psylla(Cacopsylla pyricola)

One of the most important pear pests where established; transmits pear disease; distributed throughout eastern states and pear-growing regions of Pacific Coast

X X X

Tobacco budworm(Heliothis virescens)

Attacks tobacco, cotton, and other plants; key secondary pest of cotton; occurs from Missouri, Ohio, and Connecticut southward; most injurious in Gulf states

X X X

Soybean looper(Pseudoplusia includens)

Major defoliator of soybean; also attacks peanut, cotton, tobacco, and other crops; occurs in southern Atlantic and Delta regions of the United States

X X X

Beet armyworm(Spodoptera exigua)

Attacks beet, alfalfa, cotton, asparagus, and other root and vegetable crops; distributed from the Gulf states north to Kansas and Nebraska and west to the Pacific Coast

X X X

Fall armyworm(Spodoptera frugiperda)

Attacks corn, sorghums, and other grass-type plants; occurs throughout Gulf states; sometimes migrates north as far as Montana or New Hampshire, but cannot survive winter

X X X

Diamondback moth(Plutella xylostella)

Attacks cabbage, and ornamental and greenhouse plants; occurs wherever its host plants are grown

X X X X

German cockroach(Blattella germanica)

Most common household roach; spreads filth; damages household items; is suspected vector of human diseases; distributed worldwide

X X X X

Cat flea(Ctenocephalides felis)

Worldwide pest of cats; common indoors in eastern United States; can carry the bacteria that causes bubonic plague

X X X X

Citrus thrips(Scirtothrips citri)

One of the most important citrus pests in California and Arizona

X X X

* OP = organophosphates; C = carbamates; P = pyrethroids; Oth = other smaller categories of pesticides, including microbial pesticides.

SOURCES: Resistance data from G.P. Georghiou, University of California, Riverside, CA, “Insecticide Resistance in the United States,” unpub-lished contractor report prepared for the Office of Technology Assessment, U.S. Congress, Washington, DC, April 1995; and data on pest impactfrom R.L. Metcalf and R.A. Metcalf, Destructive and Useful Insects: Their Habits and Control, 5th Ed. (New York, NY: McGraw Hill, 1993).NOTE: Data in table indicate where resistance has been documented in one or more locations in the United States.

TABLE 2-4: Critical Cases of Multiple Insecticide Resistance in the U.S. Today (Cont’d.)

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22 Biologically Based Technologies for Pest Control

❚ Newly Emerging Pest ThreatsThe number of pests in the United States is con-stantly growing. The 1993 OTA assessment ofHarmful Non-Indigenous Species in the UnitedStates showed that new species continuouslyflow into the country, but few previous immi-grant (or nonindigenous) pests, such as the boll-worm (Helicoverpa zea) or the European gypsymoth, are ever eradicated (338). Newly arrivedpests just since 1980 include:

m

the Russian wheat aphid (Diuraphis noxia),which has caused more than $850 million incrop losses;the zebra mussel (Dreissena spp.), whichspread to more than 17 states in less than adecade, imperiling native mussels, foulingwater intake systems, and causing losses to thepower industry that are expected to exceedseveral billion dollars; andthe Asian tiger mosquito (Aedes albopictus),which is now found in more than 22 states andis an effective vector of several serious humandiseases such as dengue fever (338).

OTA estimated that more than 205 specieswere newly detected or introduced into theUnited States from 1980 through 1993, with atleast 59 having the potential to become pests.Moreover, this rate of pest entry is expected torise with the increasing globalization of trade andadvent of more rapid methods of transportation(338). Global warming is similarly expected toincrease rates of pest entry to the United States,as species usually restricted to lower latitudesmigrate northward (338).

In addition, public authorities are now attack-ing some old pests with new vigor. Specifically,changing public values have caused increasedemphasis on the conservation of indigenousbiodiversity —the nation’s biological heritage. Innumerous parks and nature reserves, this biodi-versity is now imperiled by nonindigenousweeds, insect pests, and plant diseases that para-sitize, kill, consume, compete with, or destroythe habitats of native plants and animals.

In the late 1980s, the silverleaf whitefly (Bemisia argentifolii)emerged as a new pest in the southwestern United States,causing hundreds of millions of dollars in crop damage.

Agricultural Research Service, USDA

National Park Service managers, for example,now rank nonindigenous species as one of thetop threats to park natural resources (338). Stew-ards of Nature Conservancy lands in 46 statesreport problems with pest plants, and 59 percentof all stewards rank pest plants as one of their top10 conservation concerns (284).

Managers of natural areas are increasinglyseeking methods to suppress these pests whileleaving the native flora and fauna unharmed. Sci-entists are similarly directing increased attentiontoward dealing with introduced pests in aquaticsystems —rivers, lakes, streams, and oceans(191). The need is for effective, but highly spe-cific, pest control methods that can be used inenvironmentally sensitive habitats-criteria metby few conventional pesticides.

Nonindigenous weeds also degrade westernrangelands. A number provide only low-valueforage for cattle, and some, like leafy spurge

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(Euphorbia esula), are toxic (425). These harm-ful plants are spreading rapidly across federallands and now infest around 17 million acres.Indeed, the threats from certain nonindigenousweeds—called noxious weeds12—were deemedsignificant enough to merit special mention inthe 1990 Farm Bill,13 which amended the Fed-eral Noxious Weed Act to require the develop-ment of weed management plans on all federallands. The Secretary of the U.S. Department ofthe Interior (DoI) recently set up an agency-widetask force to aid in addressing this requirement(290). In addition, a number of DoI and USDAagencies have signed onto a Memorandum ofUnderstanding to coordinate the prevention andcontrol of noxious weeds (see also chapter 5).

12 A “noxious weed” under the Federal Noxious Weed Act, as amended (7 U.S.C.A. 2814), is “of foreign origin, is new to or not widelyprevalent in the United States, and can directly or indirectly injure crops, other useful plants, livestock, or poultry, or other interests of agri-culture, including irrigation, or navigation or the fish or wildlife resources of the United States or the public health.” A total of 93 specieshave been designated federal noxious weeds by the U.S. Department of Agriculture’s Animal and Plant Health Inspection Service. Weedexperts believe that hundreds of other species also deserve this designation (338).

13 The Food, Agriculture, Conservation, and Trade Act of 1990.

RESPONSES BY CONGRESS AND THE EXECUTIVE BRANCHThe significance of pesticide losses, pest resis-tance, and emerging pest threats has not been loston national policymakers. Congress respondeddirectly to a number of these in the 1990 FarmBill in provisions related to use and registrationof pesticides, identification of pest control tools,and control of exotic pests (box 2-4). Pesticideissues have generally remained high on the con-gressional agenda: between 45 and 152 billsdirectly or indirectly addressing pesticide issueshave been introduced into each Congress sincethe 98th Congress convened in 1985.14 In the103d Congress alone (January 1993 to January1995), 33 bills dealt directly with pesticide-related issues. Of these, 19 addressed the healthand environmental impacts of pesticides, and atleast three dealt with future need for effectivepest control methods and approaches. This inter-est continues in the 104th Congress, where eightpesticide-related bills had been introduced as ofMay 24, 1995. Two dealt with pesticide impactson health and the environment, and five withmeeting future pest control needs.

The most notable related action in the execu-tive branch of government is the Clinton Admin-istration’s June 1993 announcement of its intentto reduce the use and risks of pesticides (see alsobox 5-1 in chapter 5). A major mechanism forachieving this goal is the Administration’s statedcommitment to develop and implement IPMpractices on 75 percent of U.S. crop acreage bythe year 2000 through the actions of three federalagencies—USDA, EPA, and the Food and DrugAdministration (FDA).15 The Administration has

14 Data derived from OTA’s search of the Legislate and Scorpio databases.15 Note that this is the third administration to develop an IPM initiative (44). Under President Nixon, the Council on Environmental Qual-

ity issued an IPM policy document in 1972 and $12.5 million were allocated to the “Huffaker Project”—a research, training, and demonstra-tion program for IPM. President Carter also tasked the Council on Environmental Quality to make recommendations to facilitate expansionof IPM.

Some pests can have profound environmental impacts. Theseleafless trees in midsummer result from the European gypsymoth’s (Lymantria dispar) voracious appetite.

Agricultural Research Service, USDA

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Some pests can have profound environmental impacts. Theseleafless trees in midsummer result from the European gypsymoth’s (Lymantria dispar) voracious appetite.

Agricultural Research Service, USDA

(Euphorbia esula), are toxic (425). These harm-ful plants are spreading rapidly across federallands and now infest around 17 million acres.Indeed, the threats from certain nonindigenousweeds-called noxious weeds12—were deemedsignificant enough to merit special mention in

13 which amended the Fed-

the 1990 Farm Bill,eral Noxious Weed Act to require the develop-ment of weed management plans on all federallands. The Secretary of the U.S. Department ofthe Interior (DoI) recently setup an agency-widetask force to aid in addressing this requirement(290). In addition, a number of DoI and USDAagencies have signed onto a Memorandum ofUnderstanding to coordinate the prevention andcontrol of noxious weeds (see also chapter 5).

RESPONSES BY CONGRESS ANDTHE EXECUTIVE BRANCHThe significance of pesticide losses, pest resis-tance, and emerging pest threats has not been loston national policymakers. Congress respondeddirectly to a number of these in the 1990 FarmBill in provisions related to use and registrationof pesticides, identification of pest control tools,and control of exotic pests (box 2-4). Pesticideissues have generally remained high on the con-gressional agenda: between 45 and 152 billsdirectly or indirectly addressing pesticide issueshave been introduced into each Congress sincethe 98th Congress convened in 1985.14 In the103d Congress alone (January 1993 to January1995), 33 bills dealt directly with pesticide-related issues. Of these, 19 addressed the healthand environmental impacts of pesticides, and atleast three dealt with future need for effectivepest control methods and approaches. This inter-est continues in the 104th Congress, where eightpesticide-related bills had been introduced as ofMay 24, 1995. Two dealt with pesticide impactson health and the environment, and five withmeeting future pest control needs.

The most notable related action in the execu-tive branch of government is the Clinton Admin-istration’s June 1993 announcement of its intentto reduce the use and risks of pesticides (see alsobox 5-1 in chapter 5). A major mechanism forachieving this goal is the Administration’s statedcommitment to develop and implement 1PMpractices on 75 percent of U.S. crop acreage bythe year 2000 through the actions of three federalagencies—USDA, EPA, and the Food and DrugAdministration (FDA).

15 The Administration has

12 A “noxious weed” under the Federal Noxious Weed Act, as amended (7 U. S.C.A, 2814), is “Of foreign Origin, is new to or not widelyprevalent in the United States, and can directly or indirectly injure crops, other useful plants, livestock, or poultry, or other interests of agri-culture, including irrigation, or navigation or the fish or wildlife resources of the United States or the public health.” A total of 93 specieshave been designated federal noxious weeds by the U.S. Department of Agriculture’s Animal and Plant Health Inspection Service, Weedexperts believe that hundreds of other species also deserve this designation (338).

13 The Food, Agriculture, Conservation, and Trade Act of 1990.14 Data derived from OTA’s search of the Legislate and Scorpio databases.15 Note that this is the third administration to develop an 1PM initiative (44), Under President Nixon, the Council On Environmental Qual-

ity issued an IPM policy document in 1972 and $12.5 million were allocated to the “Huffaker Project”-a research, training, and demonstra-tion program for 1PM, President Carter also tasked the Council on Environmental Quality to make recommendations to facilitate expansionof 1PM.

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not specified its interpretation of IPM, but thegoal of expanding IPM is to reduce the use ofpesticides by making a broader array of pestmanagement tools and techniques available tofarmers (84).

The executive branch’s national IPM initiativeencompasses a number of different actions (401).EPA and USDA signed a memorandum ofunderstanding in August 1994 to provide theagricultural community with pest management

BOX 2-4: Congress Anticipates Future Pest Control Needs in the 1990 Farm Bill

Registering pesticides for minor use crops

Title XIV—Conservation; Subtitle H—Pesticides: Amends the Federal Insecticide, Fungicide, and

Rodenticide Act to allow the EPA Administrator to reduce or waive the fee for registration of a minor usepesticide if that fee “would significantly reduce the availability of the pesticide for the use.”

Reducing pesticide use

Title XIII—Fruits, Vegetables, and Marketing; Subtitle C—Cosmetic Appearance: Directs the Secretary

of Agriculture to conduct research to determine impacts of federal grade standards and other regulationson pesticide use on perishable commodities, and to determine the impacts of reducing emphasis on cos-

metic appearance in grade standards and other regulations on “the adoption of agricultural practicesthat result in reduced pesticide use.”

Identifying and developing pest control tools to fill fu ture needs

Title XIV—Conservation; Subtitle D—Other Conservation Measures: Directs federal agencies todevelop programs for control of undesirable plants (including noxious weeds) on federal lands and for

related “integrated management systems” based on education, prevention, and control by physical,chemical, and biological methods.

Title XIV—Conservation; Subtitle H—Pesticides: Directs the EPA Administrator in cooperation with the

Secretary of Agriculture to identify available methods of pest control by crop or animal; minor pest controlprograms (either problems in minor crops or small problems in major crops); and factors limiting the

availability of pest control methods (such as resistance and regulatory actions). Requires the Secretary ofAgriculture to identify crucial pest control needs where a shortage of control methods occurs and to

describe in detail research and extension designed to address these needs.

Directs the Environmental Protection Agency Administrator and the Secretary of Agriculture to develop

approaches to pest control, based on integrated pest management and emphasizing minor pests, thatrespond to the needs of producers.

Requires the National Academy of Sciences to conduct a study of the biological control programs and

registration procedures used by the Food and Drug Administration, the USDA Animal and Plant HealthInspection Service, and the EPA. Directs these federal agencies to develop and implement a common

process for reviewing and approving biological control applications.

Title XVI—Research; Subtitle F—Plant and Animal Pest and Disease Control Program: Directs the Sec-retary of Agriculture to set priorities designed to overcome shortages in its pest and disease control

research and extension programs where data indicate a shortage of available pest or disease controlmaterials or methods to protect a particular crop or animal.

Directs the Secretary of Agriculture to expand research and grant programs related to exotic (non-indigenous) pests to improve existing methods (i.e., sterile release), develop safer pesticides (e.g., pher-

omones), and develop new methods of pest control.

SOURCE: Compiled by the Office of Technology Assessment, 1995, from the Food, Agriculture, Conservation, and Trade Act of1990, P.L. 101–624.

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practices that reduce pesticide risks. Accordingto this agreement, USDA will increase itsresearch on alternative pest control tools andmeans of transferring these tools to farmers. Inaddition, USDA and EPA will work together 1)to identify crop/pest situations in which pest con-trol tools will become unavailable because ofregulatory action, a lack of alternatives, or pestresistance and 2) to expedite research, develop-ment, education, and registration to attack theseproblems.

Specific programs are now being developed tomeet the general goals just identified. USDA hasassembled an IPM Coordinating Council withmembership from all eight USDA agencies thathave related responsibilities, and has requestedapproximately $22 million in fiscal year 1996funding for related programs. A major part of theUSDA effort will be a program to assembleteams composed of farmers, researchers, exten-sion staff, crop advisors, and others to developcrop-specific IPM systems. This will be fundedthrough the Cooperative State Research, Educa-tion, and Extension Service (CSREES). EPA haslaunched a pilot Biopesticides and Pollution Pre-vention Division to facilitate registration of bio-logical pesticides, administer EPA’s IPMprogram, and develop activities to prevent pesti-cide pollution.

DEFINING THE TERMS OF OTA’S ASSESSMENTThe five kinds of biologically based technologies(BBTs) covered in this assessment represent animportant segment of the alternatives to conven-tional pesticides (presented earlier in box 2-1)and a significant part of USDA’s emphasis inpest control. The majority of the “safer” pesti-cides that EPA is promoting to reduce the risksof pesticide use are microbial pesticides andpheromone-based products; these two categoriesmade up 45 percent of all new active pesticidalingredients registered by EPA in 1994 (401).

OTA’s assessment of BBTs thus provides a“bottom-up” view of whether the national infra-structure supporting research, development, and

implementation can support diversification ofpest control technologies and expansion of IPM.Box 2-5 describes in greater detail several addi-tional technologies not within OTA’s scope thatare receiving increased attention for the samereasons as BBTs.

Most activity related to BBTs has occurredwithin the agricultural sector. Pests plague allareas of human activity, and the forces affectingthe availability of pest control in the future willaffect nonagricultural areas as well. The OTAassessment thus examines application of BBTs tothe full array of pest problems, ranging fromagriculture, rangelands, and forestry, to parksand wilderness preserves, urban and suburbanenvironments, and even aquatic habitats.

❚ A Caution on TerminologyA multitude of terms characterize the field ofbiologically based pest control. Moreover, thesame terms are used with somewhat differentmeanings among varying subdisciplines (e.g.,insect pest management versus plant diseasemanagement) (15). Although some of these dif-ferences seem esoteric to nonspecialists, unfa-miliar uses of terms can arouse strong feelingsamong scientists, in part because research fund-ing is often tied to specific definitional interpre-tations (15). Moreover, some definitionalniceties reflect underlying philosophical beliefsabout the most appropriate approach to pest man-agement.

The best known example of such controversyoccurred in response to the report from aNational Academy of Sciences working group(243). That report broadened the definition ofbiological control beyond the use of livingorganisms to include the use of genes or geneproducts to reduce pest impacts. All of the tech-nologies within OTA’s scope would fall withinthis definition, as might naturally derived botani-cal pesticides and insect growth regulators (box2-1). Adherents to the historical, narrower inter-pretation of biological control worried that other,newer approaches might garner a disproportion-ate share of research dollars at the expense of

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BOX 2-5: Technologies Not Covered in This Assessment Also Receiving Increased Attention

Botanical pesticides

“Botanicals” are chemicals derived from plants that are used in the same way as conventional pesti-

cides. They can be either naturally occurring or synthesized. Examples include pyrethroids originally fromchrysanthemum flowers and nicotine from tobacco. Naturally occurring botanicals enjoy popularity

among organic farmers and gardeners because they are derived from “natural” sources. However, scien-tists believe that botanicals are no safer as a group than synthetic chemicals and pose the same ques-

tions of mammalian toxicity, carcinogenicity, and environmental impact.

Insect growth regulators (IGRs)

IGRs are naturally occurring hormones or similar synthesized compounds that influence insect growth.Insects repeatedly shed and then form a new outer layer as they grow in a process called molting. IGRs

kill insects by interfering with the molting process. These insecticides have low toxicity to mammals, butsome IGRs affect crabs, shrimp, and other animals that molt. Concerns about nontarget impacts on these

other species, some of which are economically important, have led to stringent restrictions on alloweduses of IGRs. IGRs are now being examined with renewed interest for use in environments where such

nontarget impacts are highly unlikely, such as in homes or grain storage elevators. More specific IGRsmight be developed for high-dollar pests; however, no species-specific IGRs are presently on the market.

Plant breeding and enhanced resistance to pest damage

For centuries, humans have selected the most hardy strains of crop plants to propagate and grow.Significant reductions of pest damage to plants in agriculture and landscapes can be attributed to the

efforts over the past few decades of plant breeders who have developed pest-resistant plant cultivars.Recent advances in genetic engineering have greatly enhanced the possibilities in this area by enabling

the transfer of genes that confer resistance to pests between widely unrelated organisms. The newgenetic engineering techniques bring great promise, but also certain risks. A number of important issues

remain unresolved in the policy arena, such as food safety effects, potential transfer of genes to weedyspecies, the appropriate venue and standards for regulation, and the ability of pests to evolve tolerance

to the plant changes. Of particular significance is that many crop plants are being genetically engineeredto produce toxins found in Bt. Scientists worry this will speed the rate at which pests become resistant to

Bt—rendering microbial pesticides composed of the bacteria ineffective (see also chapter 4 of thisreport).

Physical, cultural, and mechanical control

These approaches either manipulate the environment to make it less conducive to pest damage, or

directly remove a pest through mechanical means. Examples include crop rotation, sanitation, choice ofplanting and harvest dates to avoid pest infestations, water management practices, and solarization

(heating soil to kill pests). Most cultural/mechanical approaches are environmentally benign, although till-age can contribute to soil erosion. Use of these approaches is widespread but patchy. They require a

knowledgeable farmer, and because most cultural/mechanical approaches do not involve a marketableproduct, sources of adequate information often are lacking. For this reason, research and development of

cultural/mechanical approaches depends primarily on the public sector.

SOURCE: Office of Technology Assessment, 1995; M.L. Flint, University of California, Davis, CA, “Biological Pest Control: Tech-nology and Research Needs,” unpublished contractor report prepared for Office of Technology Assessment, U.S. Congress,Washington DC, November 1993.

NOTE: Technologies presented here are a subset of those outside of OTA’s scope shown in box 2-1 earlier in this chapter.

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their discipline (15). They also felt that someapproaches gained unwarranted legitimacy bytheir association with more “environmentallyfriendly” biological control: microbial pesticidesbased on Bt, for example, kill pests by a toxin,and, according to these critics, perpetuate themind-set of a pesticide-based approach (see alsobox 2-2). This debate, which continues today,was the focus of considerable discussion duringan ongoing study by the National ResearchCouncil.16

❚ OTA’s Definitions of Technologies Covered in This AssessmentOTA’s selection of the definitions here balancesa straightforward conceptual presentation withpolicy relevance and commonly accepted usageamong scientists and other professionals. Thegoal is to clarify the presentation of this reportwhile retaining scrupulous technical accuracy.The definitions are not necessarily intended fordirect incorporation into statutes, regulations, orpolicy statements.

Biological ControlPopulations of all living organisms are, to somedegree, reduced by the natural actions of theirpredators, parasites, competitors, and diseases.Scientists refer to this process as biological con-trol and to the agents that exert the control (i.e.,predators, parasites, competitors, and patho-gens17) as natural enemies.18 Humans canexploit biological control in various ways to sup-press pest populations. These approaches differin how much effort is required, who is involved,and how suitable the approach is for commercialdevelopment.

16 The NRC’s Board on Agriculture has an ongoing study of “Pest and Pathogen Control Through Management of Biological ControlAgents and Enhanced Natural Cycles and Processes.” The report, scheduled for publication in late 1995, discusses issues related to necessarytypes of research, and complements but does not duplicate the OTA assessment.

17 Pathogens are disease-causing agents, including certain bacteria, viruses, fungi, protozoa, and nematodes (microscopic worm-like ani-mals).

18 Natural enemies are also sometimes referred to as beneficial organisms. Use of this term can be confusing because some organisms,like honeybees, are beneficial organisms but are not natural enemies.

Some organisms become significant pestsonly when they move to a new locale where theirnatural enemies are absent and therefore theorganism’s population expands greatly. Oneapproach to managing these nonindigenous pestsis to reestablish control by importing and releas-ing natural enemies from the pest’s region of ori-gin. Termed classical biological control19 byspecialists, the goal is permanent establishmentof the natural enemies in the new locale. Throughreproduction and natural spread, the controlagents can then effectively “track” the pestthroughout all or part of its new range and pro-vide enduring pest suppression with little or noadditional effort. Classical biological control isgenerally regarded as a public-sector activityhaving little potential for commercial involve-ment. Researchers from universities and federaland state government are the primary peopleinvolved in the discovery, importation, andrelease of classical biological control agents.Many farmers, homeowners, and other users ofpest control products are unaware of the extent towhich imported natural enemies now keep cer-tain potential pests in check, obviating or reduc-ing the need to use additional control measures.Examples of such pests are the woolly appleaphid (Eriosoma lanigerum) of the PacificNorthwest, the sugarcane delphacid (Perkinsiellasaccharicida) in Hawaii, and the weed St. John’swort (Hypericum perforatum) in the westernUnited States, all of which are currently under asignificant level of biological control.

Some natural enemies, both imported andindigenous, can be repeatedly propagated andreleased in large numbers. These augmentative20

releases temporarily increase the natural enemy’sabundance in a specific target area and therefore

19 The term innoculative biological control is also used by some specialists (418).20 The term innundative biological control is also used by some specialists (418).

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its impact on the pest species. The temporarilyboosted abundance may far exceed that whichthe environment would normally support. Aug-mentation can also create a transient populationof a natural enemy that could not otherwise per-sist in the environment (e.g., because it cannottolerate cold winters). One potential advantage ofaugmentation is that the release can be timed tocoincide with the period of the pest’s maximumvulnerability, such as a particular larval stage. Inmost agricultural applications, augmentativereleases occur once or several times throughout agrowing season. Live microbial pesticides (dis-cussed in the next subsection) are another formof augmentative biological control. A small U.S.industry now commercially distributes and sellsinsects that are natural enemies of insect andweed pests, primarily to farmers and ranchers.Approximately 110 different species are nowcommercially available from more than 130North American companies (60). Some federaland state government agencies also make aug-mentative releases.

The action of all natural enemies—indige-nous, imported, and augmented—can beenhanced by simply encouraging their survivaland multiplication. This conservation of naturalenemies usually involves specific crop, forest, orlandscape management practices that provide thenatural enemies with a hospitable environmentand limit practices that kill natural enemies—forexample, by reducing pesticide use or selectingspecific pesticides. The practitioners of thisapproach are farmers and others who seek tocontrol pests. Usually, no commercial productsare directly involved but crop, forest, or land-scape management advisors may provide adviceto farmers, homeowners, and others about con-servation of natural enemies or other related ser-vices for a fee. Federal and state governmentsalso provide public education on such manage-ment practices through extension and outreachactivities.

Microbial PesticidesA wide variety of microorganisms (organismstoo small to be seen by the naked eye) suppress

pests by producing poisons, causing disease, pre-venting establishment of other microorganisms,or various other mechanisms. Such microorgan-isms include certain bacteria, viruses, fungi, pro-tozoa, and nematodes. A microbial pesticide is arelatively stable formulation of one or severalmicrobes designed for large-scale application.The most widely used microbial pesticide todayis Bt, formulated from the bacteria Bacillus thur-ingiensis. Its pesticidal properties result fromtoxins the bacteria produce that can kill certaininsect pests. Most microbial pesticides are pro-duced commercially and sold to farmers, forest-ers, homeowners, government agencies, andother users of pest control products.

Behavior-Modifying ChemicalsMany organisms emit chemical cues that evokespecific behaviors from other individuals of thesame or a different species. Pheromones are onecategory of these chemicals that currently hasapplication in pest management. Pheromonesserve to communicate information among mem-bers of a single species. Mate-attraction phero-mones are now used in pest lures or in traps lacedwith insecticides or microbial pesticides. Someare sold commercially for pest control, althoughthe primary function of most is monitoring ofpest distribution. The pheromone-based methodin greatest use is widespread application of pher-omones to disrupt a pest’s normal mate-findingbehavior (and thereby reduce successful repro-duction). Farmers, foresters, homeowners, andgovernment agencies rely on commercially pro-duced pheromone products.

Genetic Manipulation of PestsIn this approach individuals of the pest speciesare genetically altered and then released into thepest population. The individuals carry genes thatinterfere with reproduction or impact of the pest.The specific method in significant use today isthe release of sterile males for insect control.Males of the pest insect are made sterile by irra-diation. Following release, they compete withfertile males for female mates, thereby reducing

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the number of matings that successfully produceoffspring. The result is a drop in the size of thepest population.

Plant ImmunizationThe ability of crop and landscape plants to resistdiseases and insect pests can be enhancedthrough a number of methods that do not involveplant breeding or genetic engineering. Oneapproach of growing importance in the turfgrassindustry is the use of grass containing endo-phytes—certain fungi that live within plant tis-

sues. Plants containing these fungi are lesssusceptible to damage by insects and diseases.Researchers are working on developing methodsof transferring endophytes to plants in whichthey do not normally occur. Scientists have alsofound they can enhance resistance to disease incertain plants by exposing them to specificmicrobes or chemicals or by inoculating themwith a less-damaging strain of a disease-causingmicrobe. The various methods of inducing dis-ease and pest resistance are experimental and notyet in practical use.

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3The

Technologies

ny assessment of biologically based pestcontrol faces an immediate paradox. Awealth of technical information andresearch findings characterize the field,

and there is near uniform agreement that use ofbiologically based technologies (BBTs) is desir-able, if they can safely provide adequate pestcontrol.1 Nevertheless, actual adoption of thesetechnologies is low. Explanations for this seem-ing contradiction usually center on numerous“obstacles” that hinder adoption of BBTs—somerelated to current limits to what the technologiescan do, others to social, economic, and institu-tional impediments. This chapter begins by eval-uating BBTs and discussing difficulties in settingperformance standards for these technologies. Itthen describes current and potential uses ofBBTs in the United States and identifies the fac-tors affecting their future adoption.

EVALUATING THE TECHNOLOGIESA complex mix of technical, social, and institu-tional factors contribute to the past successes and

1 See end of chapter 2 for detailed description of the biologically based technologies discussed here and throughout the assessment.

disappointments of BBTs (box 3-1). Certainhighly effective BBTs have failed because ofeconomic factors or improper use. Straightfor-ward assessment of the technical capabilities ofBBTs according to their track record of successis thus impossible. In general, BBT adoption hasoccurred most frequently where conventionalpesticides are unavailable (e.g., because of pestresistance or small market size), unacceptable(e.g., in habitats that are environmentally sensi-tive or places where human contact is high), oreconomically infeasible (e.g., because the cost ofpesticide use is high relative to the economicvalue of the resource, as in rangelandmanagement).

❚ Comparison with Conventional PesticidesDirect appraisal of the technical capabilities ofBBTs is also complicated by the question ofwhat standards to apply. In practice, the level ofpest control set by conventional pesticides is

A

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often the benchmark used for judging othermethods. Key features of such appraisals are:

■ target range—how many pests are affected;■ kill level and rate—to what extent the pest

population is suppressed and how rapidly;■ field persistence—how long a single applica-

tion continues to provide control; and■ shelf life and stability of commercial products.

Conventional pesticides generally have a widetarget range, high kill level, rapid kill rate, longfield persistence, and extended shelf life. By anymeasure, most BBTs do not compare wellaccording to these criteria. Many BBTs have anarrower target range; act more slowly; suppress,but do not locally eliminate pests; and, if soldcommercially, have a shorter field persistenceand briefer shelf life. Exceptions to these gener-alizations do exist, of course. Classical biologicalcontrol can provide lasting pest suppression, andmicrobial pesticides applied as seed treatments

may suppress plant pathogens over a growingseason or longer (138).

Conventional pesticides are often described as“stand-alone” approaches to pest control; a sin-gle chemical provides significant suppression ofmany pests. In contrast, most BBTs affect onlyone or a few pests, and some affect only one lifestage of a pest. Pheromone mating disrupters, forexample, are “adult-based” strategies and do notaffect juvenile pests already present. Bacillusthuringiensis (Bt), in contrast, works only on thefeeding juveniles (e.g., caterpillar larvae).

The timing for effective use of many BBTs isalso relatively narrow, because it must coincidewith a particular vulnerable life stage of the pestor specific environmental conditions. Like cer-tain conventional pesticides, the effectiveness ofmany BBTs is influenced by aspects of theweather, such as temperature and humidity. Also,some are impaired by conventional pesticides;natural enemies, for example, are killed by manychemicals. As a result, recent spraying at the

CHAPTER 3 FINDINGS

■ Although conventional pesticides dominate U.S. pest management practices, biologically based tech-nologies (BBTs) have penetrated most major applications and joined the mainstream. For example,

BBTs are the method of choice for certain widespread pests like the European gypsy moth (Lymantriadispar), and have been adopted by a number of major food-processing companies.

■ Current use of BBTs is patchy, however. Adoption has occurred most frequently where conventionalpesticides are unavailable, unacceptable, or economically infeasible. In such situations, the chief

advantages of BBTs become significant assets—namely, that they reduce reliance on conventionalpesticides, have generally low impacts on human health or the environment, and, in the case of classi-

cal biological control, provide lasting and low-cost suppression of individual pests.■ Most BBTs provide partial solutions to the pest problems faced by farmers and other users and usually

must be integrated with other control techniques to provide an overall package of pest suppression.They tend to fare poorly when evaluated against the performance standards set in place by conven-

tional pesticides.■ The field of BBTs is characterized by a wealth of technical information combined with far fewer on-the-

ground applications. People involved in the research, development, and use of BBTs attribute the lowadoption to numerous technical, social, economic, and institutional obstacles. These obstacles repre-

sent real and valid impediments, but they make a precise assessment of the true capabilities andfuture potential of BBTs difficult.

■ Removal of the nontechnical obstacles through a variety of policy actions would surely improve thesuccess record of BBTs. Nevertheless, significant technical issues still need to be resolved, and this

problem can be addressed only through appropriate adjustment of the national research agenda.

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BOX 3-1: Outcomes of Biologically Based Pest Control

Some notable successes... And some disappointments

Classical biological control

Ash whitefly (Siphoninus phillyreae)—First noticed inCalifornia in 1988, the pest soon spread to 28 counties

in that state as well as to Arizona, and New Mexico. Itattacked ornamental trees that make up 17% of street

trees in urban areas. Within two years of biological con-trol introductions in 1990, the fly was under complete

control, generating net savings in excess of $200 mil-lion.

Skeletonweed (Lygodesmia juncea)—The rust fun-gus Puccinia chondrillina was released in several west-

ern states in 1976. Skeletonweed is now underexcellent control in California, Idaho, Oregon, and

Washington because of the disease.

European gypsy moth (Lymantria dispar)—Despitea century of research and introductions of over 50 dif-

ferent biological control agents, most recently in 1994,biological control has not yet been successful and

problems with the pest continue to worsen.

Augmentative biological control

Strawberries—An estimated 50 to 70% of Californiastrawberry acreage uses the beneficial mite Phytoseiu-lus persimilis against the two-spotted spider mite Tet-ranychus urticae, an important pest. Use grew rapidly

in 1987 when the widely used pesticide Plictran wasremoved from the market by federal regulation. Other

alternatives were not available and growers turned tonatural enemies.

Convergent lady beetles (Hippodamia conver-gens)—Lady beetles collected from field populations in

California have dominated the market for yard/gardenuse of natural enemies since they were first sold in the

early 1900s. Results of research on the beetles haveconsistently been disappointing, however, because

most fly away within 24 hours after they are released.Some companies are beginning to market lady beetles

“preconditioned” to ensure a more sedentary behavior,but the claims of enhanced efficacy remain to be well

documented.

(continued)

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Some notable successes... And some disappointments

Microbial pesticides

Bt—Various products based on the bacterium Bacil-lus thuringiensis are now the most widely used micro-bial pesticides in the United States and worldwide. Theprimary uses are for control of European gypsy moth(Lymantria dispar), various caterpillar pests, and theColorado potato beetle (Leptinotarsa decemlineata).

Black vine weevil (Otiorhynchus sulcatus)—In cran-berry bogs, this pest has been successfully controlledby nematodes. Favoring success were the soil condi-tions, susceptibility of the pest, safety of the product,lack of other alternatives, and high value of the crop. Inaddition, Ocean Spray, a farming cooperative that is theprimary user, worked closely with the manufacturer todevelop suitable application methods.

“Milky spore” for control of Japanese beetle (Popilliajaponica)—First introduced as a classical biologicalcontrol in the 1930s, commercial formulations of Bacil-lus popilliae became available for control of the pest inturf during the 1980s. A number of lawn care compa-nies experimented with these products, but poor qualitycontrol in production meant inconsistent product perfor-mance. As a result, lawn care company representativesdo not believe that milky spore is effective and will notuse it for control of Japanese beetle grubs. For somemembers of the industry, this experience has gener-ated a high level of distrust for microbial pesticides ingeneral.

Collego—This microbial pesticide is based on apathogen of northern joint vetch (Aeschynomene vir-ginia). First sold in 1982 by Upjohn, Inc., Collegooffered excellent control over northern jointvetch in ricefields. The product was taken over by Ecogen, but pro-duction costs rose after the change. Eventually, themarket size proved too small to justify continued pro-duction, and Collego was withdrawn from the market in1994.

Elcar—This viral insecticide was developed by San-doz, Inc. for use against the bollworm (Helicoverpa zea)where resistance to conventional pesticides was occur-ring. The virus was very effective and its initial pros-pects were good. But entry of pyrethroids onto themarket at about half the price of the virus turned it into afinancial disaster, and Elcar was removed from the mar-ket. Interest in this approach is reemerging because thebollworm is developing resistance to pyrethroids aswell.

(continued)

BOX 3-1: Outcomes of Biologically Based Pest Control (Cont’d.)

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Chapter 3 The Technologies | 35

control site or drift of pesticides from adjacentareas can affect performance of certain BBTs.

For these reasons, BBTs do not provide a highenough level or broad enough range of pest sup-pression to satisfy the full needs of farmers andother users whose expectations have been set byconventional pesticides. BBTs thus need to beused in a more integrated fashion with other con-trol techniques to provide an overall package ofpest suppression. This requirement means that

the performance of BBTs may often depend onthe quality of the specific integrated pest man-agement (IPM) system in use—whether it dealswith the full range of likely pest problems andcan respond to changing pest control needs.

❚ An Important Benefit of BBTsSome of the very characteristics that make BBTscompare poorly with conventional pesticidesbecome advantages in pest management systems

Some notable successes... And some disappointments

Pheromone-based products

Pink bollworm (Pectinophora gossypiella)—Matingdisruption approaches on 27,000 acres of the Parker

Valley in Arizona starting in 1989 resulted in a decreaseof damage to cotton bolls from 25% (with standard

regime of conventional pesticides) to 0% (with the pher-omone approach).

European elm bark beetle—Attempts to mass-trapthe beetle, the vector of Dutch elm disease, have been

unsuccessful because they do not attract enoughinsects or attract them only after the damage has

occurred.Codling moth (Cydia pomonella)—Several products

are available but the level of fruit protection achievedvaries with the product, the initial level of infestation,

and the distance of the orchard from sources of matedcodling moth females. Inconsistent formulation and

poor choice of application sites appear to be sources ofthe variable outcomes in farm-by-farm application.

Researchers believe greater success is likely using anareawide management approach.

Sterile insect approach

Screwworm (Cochliomyia hominivorax)—Large-

scale releases of sterile males, starting in the 1950s,effectively eliminated the pest from the United States

and northern Central America.

Mediterranean fruit fly (Ceratitis capitata)—The suc-

cess or failure of this approach in the Los Angelesbasin is unknown and a source of controversy among

scientists. As of November 1994, this pest was stillpresent despite releases of 14 billion sterile flies in

1993.

SOURCES: Office of Technology Assessment, U.S. Congress, 1995; W. Cranshaw, Department of Entomology, Colorado State University,Fort Collins, CO, “Biologically Based Technologies for Pest Control: Urban and Suburban Environments,” unpublished contractor report pre-pared for the Office of Technology Assessment, U.S. Congress, Washington, DC, 1994; K. Jetter and K. Klonsky, Department of Economics,University of California, Davis, CA, “Economic Assessment of the Ash Whitefly (Siphoninus phillyreae) Biological Control Program,” unpub-lished contractor report prepared for the California Department of Food and Agriculture, Sacramento, CA, June 30, 1994; “Milky Spore Dis-ease May Not Be Effective Biological Control for Grubs,” Turf Grass Trends 13, May 1994; J. Randall and M. Pitcairn, Exotic SpeciesProgram, The Nature Conservancy, Galt, CA and the Biological Control Program, California Department of Food and Agriculture, Sacra-mento, CA, “Biologically Based Technologies for Pest Control in Natural Areas and Other Wildlands,” unpublished contractor report preparedfor the Office of Technology Assessment, U.S. Congress, Washington, DC, November 1994; R. Van Driesche et al., Department of Entomol-ogy, University of Massachusetts, Amherst, MA, “Report on Biological Control of Invertebrate Pests of Forestry and Agriculture,” unpublishedcontractor report prepared for the Office of Technology Assessment, U.S. Congress, Washington, D.C., December 1994.

BOX 3-1: Outcomes of Biologically Based Pest Control (Cont’d.)

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36 Biologically Based Technologies for Pest Control

that seek to minimize pesticide inputs. Such sys-tems usually involve monitoring (scouting) ofpests so that pesticides are applied only whenoutbreaks occur.

To most people, this concept is simple: Killingpests stops their unwanted effects. To experts,however, this simplicity masks underlying com-plexity. The harmful effects of a pest are directlyrelated to its abundance. If a potential pest isnever abundant enough, its harmful effects mayremain at an acceptable level or perhaps undetec-ted. Many pest control practitioners today inter-vene only to control a pest when it reaches athreshold abundance where unacceptable effectsare likely to occur (figure 3-1; see table 2-2 inchapter 2). Potential pests sometimes remainbelow this level because of the action of natu-rally occurring biological control agents or otherfactors, such as weather.

The BBTs covered in this assessment includepractices to enhance naturally occurring controlwhen a pest is below its threshold (i.e., conserva-

tion of natural enemies) and intervention meth-ods to push pest abundance back below thethreshold (i.e., microbial pesticides). The distinc-tion between the two is somewhat fuzzy becausecertain BBTs, such as augmentative biologicalcontrol, can be used both to prevent and controlpest outbreaks (i.e., when pest densities are eitherbelow or above the threshold abundance in figure3-l).

Conventional pesticides also have been usedin both ways. A major difference between BBTsand conventional pesticides concerns the ways inwhich they affect naturally Occurring control.Many conventional pesticides kill natural ene-mies as well as pest organisms. Certain pests thatotherwise might be kept below threshold levelsby natural enemies subsequently surge to out-break levels (see box 2-2). In contrast, the speci-ficity of BBTs means they are far less likely toharm natural enemies. These technologies thusare more compatible with pest management sys-

<Economic, aesthetic,or other threshold atwhich intervention

becomes required toreduce the pest damageto an acceptable level

Time

— Pest abundance at a particular time

Below the threshold, biological control and otherfactors prevent unacceptable levels of economicor aesthetic damage.

SOURCE: Adapted by OTA from J.K. Waage, Director, International Institute of Biological Control, Ascot Berks, UK, letter to the Office of Technol-

ogy Assessment, US. Congress, Washington DC, July 14, 1995.

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tems that seek to maximize naturally occurringpest control and to minimize pesticide inputs.

❚ Gaps in the InformationThe patchy implementation of BBTs to datemeans that no precise evaluation of their capabil-ities is possible. Existing data focus more fre-quently on BBTs successes than on lessonslearned from failures—and in many cases, thenecessary long-term followup for evaluatingimpacts or effectiveness in IPM programs islacking.

An additional problem arises because so muchof the information on BBTs comes from researchresults. Scientists do not always use the termcontrol to mean a level of pest suppression that isapplicable to actual field applications. Moreover,because field conditions can greatly alter theimpacts of BBTs, research findings can not bedirectly translated into predictions about poten-tial effectiveness under conditions of practicaluse (175). This problem is especially significantfor areas like plant pathogen control, where veryfew BBTs are yet in place (308).

❚ What We Do Know about the Effectiveness of BBTs

Biological ControlWhen successful, classical biological controlprograms in which the natural enemy of a pest isidentified, imported, and released, can providelasting, highly selective, and effective control.Some programs have caused 100- to 1,000-folddrops in pest density (411). Not all biologicalcontrol programs are successful, however. In1990 it was estimated that the 722 biologicalcontrol agents previously introduced in theUnited States had resulted in some level of sup-pression for 63 arthropod pests (123).2 Somelevel of control has resulted for 21 U.S. weeds as

2 No readily available data show what proportion this figure represents of all U.S. arthropod pests against which classical biological con-trol has been attempted. On a worldwide basis, for all pests targeted by classical biological control programs, approximately 16 percent arenow completely controlled and another 40 percent are partially controlled by this method (411). Note that several natural enemies may beintroduced before control occurs, and a project against a single pest can take anywhere from a few years to several decades.

a result of classical biological control introduc-tions against 51 target species (420).

Results of classical biological control pro-grams are usually reported as “complete,” “sub-stantial,” or “partial” control (69,123,153).Complete control usually refers to a level of pestsuppression at which no additional controls arenecessary against the pest. It is the least commonoutcome of classical biological control, repre-senting about 18 percent of all successful U.S.programs against arthropod pests (153).

Biological control successes generally occurslowly. A significant proportion of the U.S. suc-cesses in classical biological control againstarthropod pests thus far (at least 85 percent) wereaccomplished prior to 1964 (69,123,153). Expe-rience indicates that only about a half-dozenmajor successes can be expected in the UnitedStates per decade (415). Although, someresearchers attribute the recent slow rate of suc-cess to inadequate institutional support from theU.S. Department of Agriculture (USDA) sincethe 1970s (58), while others suggest that the“easier targets” have already been addressedusing this method (9). Recent successes are morecommon for weeds; only 45 percent of today’ssuccesses occurred prior to 1977 (153,420).

Successful biological control programs typi-cally report benefit-cost ratios from reduced pestimpacts and decreased use of pesticides of 10:1to 30:1, with some as high as 200:1 (162,411).These ratios do not incorporate the costs of otherfailed biological control programs (286,318).One reason for the high per-program returns isthat a successful classical biological control pro-gram can provide lasting benefits that accrueindefinitely into the future with little, if any, fur-ther investment. Many of the greatest successesin classical biological control have occurred inpermanent or semipermanent environments suchas orchards, forests, or rangelands, where perma-

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38

nent

Biologically Based Technologies for Pest Control

establishment of natural enemies is mostlikely to occur (60).

Benefit-cost ratios have been calculated forrelatively few classical biological control pro-grams because documenting program impacts isdifficult and costly (58). Little routine monitor-ing follows most biological control releases, andeffects can take five, 10, or more years tobecome apparent (191,41 1,420). Moreover, theeffectiveness of a biological control agent mayvary across the pest’s distribution because of dif-ferences in temperature, moisture, elevation, andother factors that affect survival and populationsize of the natural enemy and its target pest. Theresult can be a mosaic ranging from excellent tono control, depending on the specific site (420).

Even fewer attempts have been made to evalu-ate the overall effectiveness of repeated augmen-tative releases of natural enemies (41 1,263). Thefew scientific studies have been conducted ontoo small a scale to make accurate inferencesabout results under conditions of actual use(41 1), and scientists are divided about the feasi-bility and effectiveness of the approach(263,173), The utility of natural enemies inenclosed greenhouses is generally undisputed.Researchers vary, however, in their views as tothe potential effectiveness of augmenting naturalenemies in field crops; some believe that discern-ible levels of pest suppression result more fromthe positive impacts of reduced insecticide useon natural enemies already present in fields, thanfrom the deliberately released natural enemies.At present, high cost and quality control also areissues (e.g., are the natural enemies sold aliveand active?) (263,173). Another question con-cerns the scale at which augmentative releaseswill be most successful—on small farms, onlarge farms, or areawide. Nevertheless, compa-nies marketing natural enemies and farmers whouse these products believe they are effective anddispute scientists’ more mixed view of this tech-nique (269,59).

Augmentative use of fishes for control ofaquatic weeds and mosquitoes is a special case.These fishes can be quite effective, although theyact more slowly than pesticides and do not elimi-

Although the program to control of the boll weevil (Anthonomusgrandis grandis) relies on conventional pesticides, the pest’ssuccessful suppression in some states has resulted in greatlyreduced insecticide usage; natural enemies are now more com-mon in cotton fields and keep a number of other former insectpests under control.

Agricultural Research Service, USDA

nate pests completely. Because their use is con-fined to water bodies of sufficient size, clarity,and warmth to sustain the animals, their useful-ness is sometimes limited (191,315) For exam-ple, mosquito fish (Gambusia spp.) areimpractical for certain significant mosquito habi-tats such as tree holes, tires, and temporarilyflooded wetlands-all major sites of mosquitoreproduction (191,315). Introductions of fishesfor biological control also raise several signifi-cant ecological risk issues (see chapter 4).

Conservation of natural enemies has highlyvariable effects, depending on the specific cropand location. Quantitative estimates of impactsare impossible because the approach is rarelyused as a major and deliberate component of pestmanagement (41 1). Instead, increased effects ofnatural enemies are more often a consequence ofmanagement practices implemented for othergoals (such as reduced pesticide use) (9,411).Maximizing the conservation of natural enemiesmore widely would require the development ofextensive site-specific information (41 1). Over-all, the approach works only for pests that havepotential natural enemies (native or introduced)in the area (411).

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The most widely cited evidence for the poten-tial effects of conservation of natural enemiescomes from rice production in Asia. There, mod-ification of insecticide spray schedules toenhance the impacts of natural enemies has dra-matically reduced outbreaks of the rice brownplanthopper (Nilaparvata lugens), a destructiverice pest (411). In the United States, the mostcommon way farmers seek to conserve naturalenemies is by selecting conventional pesticidesthat have relatively low impacts on natural ene-mies (61). Biological control experts hold differ-ing views as to whether any chemical pesticidescause sufficiently low damage to natural enemiesfor this approach to be successful. Some believethat only microbial, pheromone, or cultural alter-natives will enable enhanced reliance on conser-vation of natural enemies (411).

Microbial PesticidesThe performance of various microbial pesticidesdiffers greatly, as does the degree to which thatperformance is affected by environmental condi-tions. Pesticides based on Bt are potent if appliedto the early larval stages of susceptible insectpests. Application during other stages causestheir effects to drop severely. Effectiveness alsovaries with the pest’s feeding rate; as a result,many Bt products are formulated to include feed-ing stimulants. Because Bt products can be man-ufactured using large-scale fermentationtechniques, they are less expensive to producethan many other microbial pesticides.

The various Bt-based pesticides are very spe-cific. This precision minimizes nontarget impactsbut also has disadvantages. For example, threecaterpillars—Heliothis virescens (tobacco bud-worm), Heliocoverpa zea (bollworm), andSpodoptera exigua (beet armyworm)—are fre-

quent cotton pests. Current Bt products arehighly effective against the first, less so againstthe second, and relatively ineffective against thethird (411). In general, Bt products have beenmost useful against forest caterpillars, Coloradopotato beetle (Leptinotarsa decemlineata) larvae,and a number of caterpillar pests of vegetablesand other crops. Recent evidence suggests thatcertain pests may develop resistance to Bt, whichcould limit its future utility (see chapter 4).

Nematodes that have been developed for pestcontrol products kill pests rapidly (within 48hours).3 They also show broader spectrumeffects than Bt. Control of insect pests is compa-rable, and sometimes even superior to insecti-cides, with data showing 100- to 1,000-folddrops in pest densities for such diverse organ-isms as caterpillars, aphids, armored scales, saw-flies, and whiteflies (411). Nematode productsare applied using standard spray equipment,traps, or baits; they are generally tolerant of mostpesticides and fertilizers (113). Environmentalsensitivity—nematodes need adequate moistureand temperatures from about 53 to 86 degreesFahrenheit—is a limitation of nematode prod-ucts. They have been used successfully in moistsoils but not in plant foliage. The shelf life ofnematode products ranges from three to 12months under refrigeration, but some of thenewer formulations can last up to five months atroom temperature. Although nematodes can bemass-produced, the high cost remains a problem.

Only two virus-based products are now in use,the European gypsy moth nuclear polyhedrosisvirus (NPV) and the beet armyworm NPV virus.4

Viruses, in general, are expensive to producebecause techniques do not yet exist to mass-pro-duce them without living hosts; according toindustry representatives, new production tech-

3 These include the steinernematid and heterorhabditid nematodes. Other nematodes that have not been developed for pest control pro-vide a slower rate of kill. OTA categorizes nematode-based products as a type of microbial pesticide because the nematodes involved aremicrobes (microorganisms) (276) and sold in commercial formulations (see chapter 2). Some scientists and commercial producers categorizenematodes as natural enemies in part because EPA does not regulate these products as a type of microbial pesticide (see chapter 4). The issueis largely semantic.

4 Another six have been registered for control of forest and crop pests, including two within the past year for celery looper (Anagraphafalcifera) and codling moth (Cydia pomonella).

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nologies will soon be available that allow lesscostly production. Viruses also persist in the fieldonly briefly because sunlight causes them to loseactivity. A few viruses are broader spectrum,affecting several insects in the same taxonomicfamily or order, although effects of a given viruson different species can vary (411).

Microbial pesticides based on fungi have highvirulence and are amenable to mass production.Their biggest drawback is requiring a moist habi-tat for activation. Fungus-based herbicides devel-oped thus far against weeds have been highlyhost-specific, relatively fast-acting, and lethal(420). Fungi developed for use against insectpests have broader host ranges (although nar-rower than Bt products) and are most effective athigh pest densities.

Only one microbial pesticide for plant patho-gen control has been in use for any length oftime. Galltrol suppresses the pathogen thatcauses crown gall disease (Agrobacterium tume-faciens) (138).5 However, this one product’seffectiveness provides only limited insight intothe general usefulness of microbial pesticidesagainst plant pathogens. Crown gall disease is aspecial case; because the disease results frominfection of plant wounds, the microbial pesti-cide has to be active for only a few hours whilethe plant wound closes. The plant then ceases tobe susceptible to infection (308).

Pheromones and Other ApproachesIn successful programs against pink bollworm(Pectinophora gossypiella) and oriental fruitmoth (Grapholita molesta), pheromone matingdisrupters have given results equal to or betterthan those of insecticides (41). The use of phero-mones to disrupt mating works only on pestsusing these chemicals to find mates over longdistances, such as most moths—which are a largeproportion of the most important insect pests.Pheromones are truly species specific, with each

5 About a half-dozen new microbial pesticide products for use against plant pathogens became available in 1994 and 1995.

working on only a single pest. They do not injurenatural enemies and can be combined with insec-ticides. In some cases, it may be necessary tocombine pheromones and pesticides to reducethe pest population sufficiently so that it can bemanaged with mating disruption (411). Somepheromone products have performed erraticallyin the field; the problem has been attributed topoor formulation and to labels that supply inade-quate information for proper use (41,175). Highcosts of pheromone use is another problem.

Experience with the screwworm (Cochliomyiahominivorax) program has shown that the sterileinsect approach can be quite successful. Duringthe 1970s, however, that program suffered someperiods of poor performance as a result of someunsound assumptions about the behavior of theflies; the experience underscores the importanceof basic knowledge of the pests’ life cycle andbehavior when using this approach (411). Effortsto suppress additional pests using sterile releaseshave had only limited success. Other geneticmanipulations of pests are being studied andhave not yet demonstrated their potential.

CURRENT USE OF BBTS IN THE U.S.Table 3-1 summarizes available data on currentusage of BBTs in the United States.6 Usage ofBBTs is uneven. The vast majority now in placeare for control of insect pests in arable agricul-ture (cultivated lands), forestry, and aquatic envi-ronments. However, use is growing for insectcontrol in urban and suburban settings as newnematode and pheromone bait products becomeavailable for turf and household pests. BBTshave virtually no role at present in the control ofweeds in arable agriculture, even though this iswhere approximately 57 percent of conventionalpesticide use occurs in the United States. Weedcontrol has been best addressed in rangelands,pastures, and waterways, specifically by classical

6 The focus here is on the United States because the success of a technology abroad may not necessarily translate directly into potentialfor U.S. adoption. There are marked international differences in farming practices and in important social and economic factors. For exam-ple, virus-based pesticides have achieved wider use in countries where lower labor costs keep the cost of production low.

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biological control. Few BBTs are yet in useagainst plant pathogens.

❚ ApplicationsThe goals of pest management vary with theapplication site. Application sites also differ inwho practices pest control and in the range ofavailable, acceptable, or feasible pest controltechnologies. The necessary or desired level ofpest suppression is higher under some circum-stances than others; for example, blemish-freefruit production requires very low rates of insectdamage, whereas greater pest abundance may betolerated in forests or rangelands. BBTs may beeasier to adopt in the latter circumstance becausethe technologies usually suppress, but do notlocally eliminate, pests. Other pest control tech-nologies that compete with BBTs are more com-mon in some applications, such as major crops.These factors, combined with the uneven avail-ability of BBTs, have generated today’s hit-or-miss pattern of BBT use.

Arable AgricultureCurrent use of BBTs in arable agriculture (culti-vated lands) is confined almost completely toinsect pests. A number of major food processorsand growers have begun to rely on BBTs in “bio-intensive” IPM systems (figure 3-2). From 1990to 1993, for example, the Campbell Soup Com-pany worked closely with Mexican tomato grow-ers to eliminate all uses of chemical insecticides.The resulting system combined monitoring, Bt,pheromones, and Trichogramma wasp releasesto provide comparable control of insect pests at alower cost (30).

Millions of acres of U.S. crops are currentlyprotected from one or more pests by the intro-duction of classical biological control agentswhich have provided some level of suppressionfor 63 arthropod pests (123,411). Most of thesebiological control agents were introduced sometime ago, but others are fairly recent; for exam-ple, introduction of parasites against the alfalfaweevil (Hypera postica) from 1980 through 1992

contributed significantly to a reduction in thatpest’s abundance and impacts (174).

Augmentative releases of natural enemies byfarmers occur primarily in vegetable, fruit, andnut crops (table 3-1) (377). Many of these usesare relatively recent. However, augmentation is along-standing practice in some areas. In the1930s a number of California citrus growersformed the Filmore Citrus Protective District, acooperative that now produces natural enemiesfor use against citrus pests such as mealybugsand scales on more than 9,000 acres (173).

Augmentative use of natural enemies in green-house agriculture is growing (411). The approachis widespread in Europe, where cultivation ofvegetable crops in greenhouses is more common.Greenhouse agriculture in the United Statesoccurs on only several hundred acres. The green-house industry for ornamental plants is muchlarger (valued at $2.5 billion in 1993), but thepotential for use of natural enemies here is lowerbecause less pest damage is tolerated on theproducts and new chemicals may provide signifi-cant competition (box 3-2) (411).

Few data quantify how frequently farmersdeliberately modify farming practices to con-serve natural enemies on U.S. croplands. Inter-cropping, modification of cropping practices,and selection of crop varieties to enhance naturalenemies all look promising to researchers buthave not been widely adopted (411). Some Cali-fornia vineyards and almond growers report thatcertain vegetation practices enhance natural ene-mies of arthropod pests and plant pathogens(257,258). Other management practices that inci-dentally conserve natural enemies are morebroadly used. One example is the routine moni-toring of natural enemies and pests in commer-cial orchards; farmers delay use of insecticides ifthe ratio of predators to pests is high enough toprevent pest damage (411). Vegetable, potato,and cotton growers commonly consider theeffects of pesticides on natural enemies whendeciding which chemicals to use and when toapply them (table 3-1) (377). Similar practicesare widespread among Pennsylvania apple grow-ers (282).

Page 49: Biologically Based Technologies for Pest Control

42 Biologically Based Technologies for Pest Control

Legal Company policies on pesticide residuesa ZeroLimits Residue

Tri Valley Growers

Dean Foods (WA)

Kraft Dean Foods (CA)

Sunkist Dole E.J. Gallo Winery

DelMonte Contadina (Nestle) Hunt-Wesson Dean Foods(TX)

Fetzer Winery

Campbells Gerbers

Heinz Nutrilite

I

Increasing use of biointensive 1PM

SOURCE: Off Ice of Technology Assessment workshop on The Role of the Private Sector in Biologically Based Technologies for Pest Control,

Washington, DC, September 20-21, 1994.NOTE: The term biointensive IPM refers to an 1PM system designed to increase plant health, This goal is generally obtained through the use of

BBTs for pest control in addition to other crop management practices. This figure was presented during the OTA Workshop on the Role of the Pri-

vate Sector. It is included here for illustration purposes only, OTA makes no claim as to the accuracy of the data.a Assignment along this continuum is based upon the company’s stated policy regarding the pesticide residue in the final shelf product and the

company’s level of use of BBTs in 1PM programs.

Page 50: Biologically Based Technologies for Pest Control

Chapter 3 The Technologies | 43

TABL

E 3-

1: A

vaila

ble

Dat

a on

the

Use

of B

BTs

in th

e U

.S.

Appl

icat

ions

Inse

ct/ i

nver

tebr

ate

pest

sW

eeds

Plan

t pat

hoge

ns

Agr

icul

ture

ar

able

cro

psB

iolo

gica

l con

trol

■63

art

hrop

od p

ests

are

und

er s

ome

leve

l of

sup

pre

ssio

n b

ycl

assi

cal b

iolo

gic

al c

ontr

ol.

■28

sta

tes

oper

ate

thei

r ow

n b

iolo

gic

al c

ontr

ol p

rog

ram

s.■

Bio

log

ical

con

trol

is u

sed

in 1

0% o

f gre

enho

uses

, 8%

of n

urs-

erie

s an

d 8

% o

f sod

pro

duc

tion.

a

■A

ugm

enta

tive

rele

ases

tak

e p

lace

on

an e

stim

ated

19%

of

the

culti

vate

d fr

uit a

nd n

ut a

crea

ge.

b

■Fa

rmer

s p

urch

ase

natu

ral e

nem

ies

for

use

on 3

% o

f the

cul

ti-va

ted

veg

etab

le a

crea

ge.

b

■M

ore

than

86

U.S

. com

pan

ies

pro

duc

e or

mar

ket n

atur

al e

ne-

mie

s w

ith a

nnua

l sal

es o

f ap

pro

xim

atel

y $9

to $

10 m

illio

n.■

Ben

efic

ial m

ites

are

used

on

an e

stim

ated

50

to 7

0% o

f C

ali-

forn

ia s

traw

ber

ry a

crea

ge.

■Fa

rmer

s ch

ang

e or

sel

ect

pes

ticid

es t

o p

rote

ct n

atur

al e

ne-

mie

s on

37%

of c

ultiv

ated

veg

etab

le a

crea

ge.

b

■G

row

ers

dec

reas

e in

sect

icid

es to

pro

tect

nat

ural

ene

mie

s on

22%

of c

ultiv

ated

acr

es o

f fal

l pot

atoe

s.b

■G

row

ers

cons

ider

nat

ural

ene

mie

s w

hen

mak

ing

pes

ticid

ed

ecis

ions

for

57%

of c

ultiv

ated

cot

ton

acre

age.

b

Bio

logi

cal c

ontr

ol■

No

wee

ds

are

curr

ently

und

er c

lass

ical

bio

log

i-ca

l con

trol

.■

No

aug

men

tativ

e b

io-

log

ical

co

ntro

l ag

ents

are

avai

lab

le.

Mic

robi

al p

estic

ides

c

■B

t-b

ased

mic

rob

ial p

estic

ides

are

use

d o

n ve

geta

ble

cro

ps,

pot

atoe

s, c

otto

n an

d c

orn.

■46

% o

f ne

mat

ode

sale

s in

199

3 w

ere

for

use

on a

rab

lecr

ops.

d

Mic

robi

al p

estic

ides

■N

o m

icro

bia

l p

esti-

cid

es a

re n

ow o

n th

em

arke

t.e

Mic

robi

al p

estic

ides

■Tw

o m

icro

bia

l p

estic

ides

hav

e an

nual

sale

s ex

ceed

ing

$10

0,00

0 fo

r cr

own

gal

l d

isea

se

( Ag

rob

acte

rium

tum

efa-

cien

s).

■Th

ree

mic

rob

ial

seed

tre

atm

ents

wer

efir

st s

old

in 1

994

for

seed

pla

nted

on

3to

5 m

illio

n ac

res

of c

otto

n, p

eanu

ts,

and

bea

ns.

■Th

ree

new

mic

rob

ial p

rod

ucts

for

con-

trol

of

pos

thar

vest

dis

ease

s b

ecam

eav

aila

ble

in 1

994

and

199

5.

(con

tinue

d)

Page 51: Biologically Based Technologies for Pest Control

44 | Biologically Based Technologies for Pest Control

Appl

icat

ions

Inse

ct/ i

nver

tebr

ate

pest

sW

eeds

Plan

t pat

hoge

ns

Phe

rom

ones

■In

199

4 th

ere

wer

e 20

reg

iste

red

, co

mm

erci

ally

ava

ilab

lep

hero

mon

e fo

rmul

atio

ns

for

the

cont

rol

of

over

20

m

oth

pes

ts.

■P

hero

mon

e p

rod

ucts

are

use

d o

n 37

% o

f th

e cu

ltiva

ted

fru

itan

d n

ut a

crea

ge.f

■P

hero

mon

e p

rod

ucts

are

use

d o

n 7%

of

the

culti

vate

d v

ege-

tab

le a

crea

ge.

f

■P

hero

mon

es

wer

e us

ed

agai

nst

orie

ntal

fru

it m

oths

on

app

roxi

mat

ely

10,0

00 a

cres

of p

each

and

nec

tarin

e or

char

ds

in 1

990.

■In

199

3, p

hero

mon

es w

ere

used

to d

isru

pt

mat

ing

of

cod

ling

mot

hs (C

ydia

pom

onel

la)

on m

ore

than

24,

000

acre

s of

ap

ple

and

pea

r or

char

ds

(slig

htly

les

s th

an 5

% o

f th

e to

tal

U.S

.ap

ple

and

pea

r ac

reag

e).

■In

19

95,

phe

rom

ones

ar

e ex

pec

ted

to

b

e us

ed

on

over

81,0

00 a

cres

in

Ariz

ona

(ab

out

25%

of

the

stat

e’s

cotto

nac

reag

e).

Oth

er m

etho

ds■

Ste

rile

inse

ct

app

roac

h ha

s su

cces

sful

ly

elim

inat

ed

the

scre

ww

orm

( C

ochl

iom

yia

hom

iniv

orax

) fr

om

the

Uni

ted

Sta

tes;

the

met

hod

is

now

in u

se a

gai

nst

the

Med

iterr

anea

nfr

uit f

ly (

Cer

atiti

s ca

pita

ta) i

n C

alifo

rnia

.

Oth

er m

etho

ds■

Cro

ss p

rote

ctio

n is

bei

ng u

sed

in F

lor-

ida

on a

pilo

t ba

sis

for

cont

rol o

f citr

usd

eclin

e.

Ran

gela

nd/

uncu

ltiva

ted

past

ures

/ fo

rest

s

Bio

logi

cal c

ontr

ol■

500,

000

para

sitic

was

ps

wer

e so

ld fo

r g

ypsy

mot

h co

ntro

l in

1994

.

Bio

logi

cal c

ontr

ol■

18

spec

ies

of

wee

ds

are

und

er s

ome

leve

l of

sup

pre

ssio

n d

ue

tocl

assi

cal

bio

log

ical

cont

rol.

■P

rog

ram

s to

con

serv

ean

d

dis

trib

ute

natu

ral

enem

ies

oper

ate

inO

reg

on a

nd M

onta

na.

■28

nat

ural

ene

mie

s ar

eno

w

sold

b

y at

le

ast

seve

n re

tail

com

pa-

nies

fo

r au

gm

enta

tive

uses

.

(con

tinue

d)

TABL

E 3-

1: A

vaila

ble

Dat

a on

the

Use

of B

BTs

in th

e U

.S. (

Con

t’d.)

Page 52: Biologically Based Technologies for Pest Control

Chapter 3 The Technologies | 45

Appl

icat

ions

Inse

ct/ i

nver

tebr

ate

pest

sW

eeds

Plan

t pat

hoge

ns

Mic

robi

al p

estic

ides

c

■O

ne p

roto

zoan

mic

rob

ial

pes

ticid

e (N

osem

a lo

cust

ae),

pro

-d

uced

by

two

U.S

. com

pan

ies,

is in

use

for

gra

ssho

pp

er c

on-

trol

.■

For

cont

rol

of t

he E

urop

ean

gyp

sy m

oth,

in

1994

, B

t w

asus

ed o

n m

ore

than

374

,000

acr

es in

11

stat

es,

and

Gyp

chek

(a v

irus-

bas

ed p

estic

ide)

was

use

d o

n ne

arly

6,0

00 a

cres

in4

stat

es.

Urb

an/

subu

rban

en

viro

nmen

ts

Bio

logi

cal c

ontr

ol■

Ash

whi

tefly

(S

ipho

ninu

s p

hilly

reae

) is

und

er c

omp

lete

con

-tr

ol b

y cl

assi

cal b

iolo

gic

al c

ontr

ol.

■N

atur

al e

nem

ies

such

as

lad

y b

eetle

s, g

reen

lace

win

gs,

and

tric

hog

ram

ma

was

ps

are

sold

to g

ard

ener

s.■

Hor

se o

wne

rs a

re a

maj

or m

arke

t for

fly

par

asite

s.M

icro

bial

pes

ticid

esc

■B

io-P

ath

roac

h b

ait

with

mic

rob

ial

pes

ticid

e ha

s b

een

mar

-ke

ted

sin

ce 1

993

for

cont

rol o

f coc

kroa

ches

.■

Hom

eow

ners

rep

rese

nted

35%

of

U.S

. ne

mat

ode

sale

s in

1993

.d

■B

t is

sol

d f

or c

onsu

mer

use

ag

ains

t g

ard

en p

ests

and

mos

-q

uito

es.

■Fo

ur f

orm

ulat

ions

of

the

fung

us B

eauv

aria

bas

sian

a b

ecam

eav

aila

ble

in 1

995

for

cont

rol o

f orn

amen

tal a

nd tu

rf p

ests

.

Mic

robi

al p

estic

ides

■O

ne m

icro

bia

l pes

ticid

e is

mar

kete

d to

pro

tect

nur

sery

pla

nts,

suc

h as

ros

eb

ushe

s an

d o

ther

orn

amen

tal

pla

nts,

from

cro

wn

gal

l dis

ease

.■

Two

mic

rob

ial

pes

ticid

es

bec

ame

avai

lab

le i

n 19

95 f

or u

se a

s a

gre

en-

hous

e so

il am

end

men

t an

d

gol

fco

urse

inoc

ulan

t.P

hero

mon

es■

Phe

rom

one

stic

ky t

rap

s ar

e so

ld i

n g

ard

en c

ente

rs f

or

use

agai

nst m

oth

pes

ts a

nd J

apan

ese

bee

tles

( Pop

illia

jap

onic

a).

Aqu

atic

en

viro

nmen

tsB

iolo

gica

l con

trol

■C

omp

etito

r sn

ails

are

wid

ely

used

in P

uert

o R

ico

for

cont

rol

of s

nails

that

car

ry h

uman

dis

ease

.■

At l

east

thre

e fis

hes

are

used

for

mos

qui

to c

ontr

ol.

■A

t le

ast

seve

n aq

uacu

lture

fac

ilitie

s co

mm

erci

ally

sel

l m

os-

qui

to fi

sh.

■Tw

o fis

hes

are

used

to c

ontr

ol n

uisa

nce

fish.

Bio

logi

cal C

ontr

ol■

Thre

e sp

ecie

s ar

eun

der

so

me

leve

l of

sup

pre

ssio

n d

ue

tocl

assi

cal

bio

log

ical

cont

rol.

■G

rass

car

p h

ave

bee

nre

leas

ed i

nto

lake

s/riv

-er

s/st

ream

s of

35

stat

es.

■Li

mite

d u

se i

s m

ade

ofot

her

fishe

s fo

r w

eed

cont

rol.

(con

tinue

d)

TABL

E 3-

1: A

vaila

ble

Dat

a on

the

Use

of B

BTs

in th

e U

.S. (

Con

t’d.)

Page 53: Biologically Based Technologies for Pest Control

46 | Biologically Based Technologies for Pest Control

Appl

icat

ions

Inse

ct/ i

nver

tebr

ate

pest

sW

eeds

Plan

t pat

hoge

ns

Mic

robi

al p

estic

ides

c

■B

t-b

ased

mic

rob

ial

pes

ticid

es a

re i

n us

e fo

r m

osq

uito

and

bla

ckfly

con

trol

.

a B

ased

on

a lim

ited

sur

vey

by

the

US

DA

NA

PIA

P p

rogr

am; t

he m

eani

ng o

f bio

log

ical

con

trol

was

uns

pec

ified

.b B

ased

on

exte

nsiv

e su

rvey

by

the

US

DA

Eco

nom

ic R

esea

rch

Serv

ice.

The

sur

vey

used

the

ter

m b

enef

icia

l, bu

t d

id n

ot s

pec

ify t

he m

eani

ng.

Gro

wer

s m

ay h

ave

incl

uded

bee

s in

the

irre

spon

ses.

Thi

s is

a s

igni

fican

t pro

ble

m fo

r in

terp

retin

g d

ata

on fr

uits

and

nut

s, b

ut le

ss s

o on

veg

etab

les

and

cot

ton.

c Ann

ual U

.S. s

ales

of m

icro

bia

l pes

ticid

es a

re b

etw

een

$60

mill

ion

to $

100

mill

ion

annu

ally

, mos

tly fo

r use

in a

gric

ultu

re a

nd fo

rest

ry. S

ome

249

mic

robi

al p

estic

ides

are

now

reg

iste

red

with

EP

A.

This

num

ber

doe

s no

t, ho

wev

er, i

ndic

ate

how

man

y ar

e cu

rren

tly p

rod

uced

com

mer

cial

ly o

r the

ir le

vel o

f use

.d

Nem

atod

es w

ere

sold

for

cont

rol o

f 33

inse

ct p

ests

on

40,0

00 a

cres

in 1

993.

Thi

s w

as e

xpec

ted

to in

crea

se to

88,

000

acre

s fo

r 199

4. T

he m

arke

t can

be

bro

ken

dow

n to

35%

for

hom

eow

ners

,46

% fo

r m

inor

use

cro

ps,

and

2%

mis

cella

neou

s.e B

ased

on

exte

nsiv

e su

rvey

by

the

US

DA

Eco

nom

ic R

esea

rch

Ser

vice

. Phe

rom

one

use

coul

d in

clud

e m

onito

ring

and

con

trol

met

hod

s.f T

wo

pro

duct

s fo

rmer

ly w

ere

on th

e m

arke

t in

the

Uni

ted

Stat

es, C

olle

go

for

cont

rol o

f nor

ther

n jo

int v

etch

(Aes

chyn

omen

e vi

rgin

ia)

and

DeV

ine

for

cont

rol o

f citr

us s

tran

gle

r vin

e (M

orre

nia

odo-

rata

). A

lthou

gh e

ffect

ive

agai

nst

thei

r in

tend

ed ta

rget

s, n

eith

er c

ould

sus

tain

larg

e en

oug

h m

arke

ts t

o ju

stify

con

tinue

d p

rod

uctio

n. D

eVin

e ha

s ju

st r

ecen

tly b

een

put

bac

k on

the

mar

ket

by

Ab

bot

t Lab

orat

orie

s as

a r

esul

t of c

oop

erat

ive

effo

rts

with

EP

A.

SOU

RC

ES:

Com

pile

d b

y th

e O

ffice

of T

echn

olog

y A

sses

smen

t, U

.S.

Con

gre

ss,

1995

, fr

om:

R.

Car

and

A.

Min

ks,

“Con

trol

of M

oth

Pes

ts B

y M

atin

g D

isru

ptio

n: S

ucce

sses

and

Con

stra

ints

,”A

nnua

l Rev

iew

of E

ntom

olog

y 40

:559

-585

, 199

5; D

.J. G

reat

head

and

A.H

. Gre

athe

ad, “

Bio

log

ical

Con

trol o

f Ins

ect P

ests

By

Inse

ct P

aras

itoid

s an

d P

reda

tors

: Th

e B

ioca

t Dat

abas

e,”

Bio

cont

rol

New

s an

d I

nfor

mat

ion

13(4

):61

N-6

8N,

1992

; C

.D.

Hun

ter,

Sup

plie

rs o

f B

enef

icia

l Org

anis

ms

in N

orth

Am

eric

a (S

acra

men

to,

CA

: C

alifo

rnia

Env

ironm

enta

l P

rote

ctio

n A

gen

cy,

1994

); A

. K

uris

,D

epar

tmen

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Chapter 3 The Technologies 47

Chloronicotinyls (synthetic nicotines) are one of the newest classes of insecticides. The first of these,

imidacloprid, was marketed by the Miles Corporation in 1994. The chemical has several useful qualities. It

diffuses throughout a plant after being applied to the roots and can persist in woody tissues for weeks or

years. Many plant-feeding insects are susceptible. Perhaps most important, imidacloprid is thought to be

relatively nontoxic to humans. Finally, it moves slowly through soils—enhancing its insecticidal impact

and diminishing the risk of groundwater contamination.

The effect of imidacloprid and related chemicals is likely to be a reduction in use of BBTs. This effect

has already been seen in the poinsettia industry, where several greenhouses being set up for biological

control of whiteflies in 1994 opted instead to use potting mix treatments of imidacloprid. If experience is

any guide, at least one important greenhouse pest—the silverleaf whitefly (Bemisia argentifolii) --is likely

to develop resistance to imidacloprid within a few seasons, This situation will again stimulate interest in

BBTs.

SOURCES: W. Cranshaw, Department of Entomology, Colorado State University, Fort Collins, CO, “Biologically Based Technolo-gies for Pest Control: Urban and Suburban Environments, ” unpublished contractor report prepared for the Office of Technology

Assessment, U.S. Congress, Washington DC, 1994; R. Van Driesche et al., Department of Entomology, University of Massachu-

setts, Amherst, MA, letter to the Office of Technology Assessment, US. Congress, Washington D. C., July 1995.

Microbial pesticides based on Bt are by far themost commonly used in agriculture. They arefrequently the method of choice when a pestdevelops resistance to chemical control methods(41 1). The major uses are for pests of vegetablecrops, with recent increases in use on potatoes,cotton, and corn following the discovery of newBt strains and development of new deliverymethods (411). Increases on cotton relate, in part,to the tobacco budworm’s development of resis-tance to pyrethroids (41 1). Some 1PM programsintegrating Bt show economic returns equivalentto those of conventional pest control programsbecause pesticide costs decline in the Bt pro-grams (41 1).

Until recently, Bt-based products were theonly microbial pesticides available for useagainst arthropod pests. The fungus Beauvariabassiana has now been formulated for useagainst a variety of pests, including grasshop-pers, Mormon crickets (Anabrus simplex),locusts, whiteflies, aphids, thrips, mealybugs,leafhoppers, psyllids, and mites. Two productsby Troy Biosciences based on this fungus, Natu-ralis-O and Naturalis-T, have recently come onthe market. Two other products, Mycotrol-GM

Microbial pesticides based on the bacterium Bacillus thurin-giensis, or Bt, are the most common ones in use today.

Agricultural Research Service, USDA

and Mycotrol-WP, have just been registered bythe EPA and are expected to be available soon.

Virus-based products have not been availablein the United States for control of agriculturalpests (with the temporary exception of Elcar; seebox 3-l). One virus product, Sped-X from Bio-sys, just came on the market for use against thebeet armyworm. NPV viruses that affect the cel-ery looper and codling moth were registered withEPA this year. Virus-based pesticides are nowused against vegetable, fruit, and cotton pests in

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48 | Biologically Based Technologies for Pest Control

China, Asia, India, Egypt, Australia, Kenya, andCentral and South America; in Brazil alone overone million acres of soybeans are treated withvirus-based pesticides each year (411).

The principal uses of pheromones today are asmating disruptants in cotton, fruit, and vegeta-bles. Aerial applications of pheromones to dis-rupt mating of the pink bollworm in the ParkerValley of Arizona led to a decline in cotton dam-age from 23.4 percent in 1989 with a conven-tional pesticide program to zero percent in 1993(411). Areawide use of the pheromone approachhas grown to an estimated 81,000 acres in 1995,or about a quarter of the state’s total acreage ofthe crop (411). Other highly successful commer-cial applications have been for the oriental fruitmoth in peaches and the tomato pinworm (Keife-ria lycopersicella). From 1991 to 1993, applica-tions of Isomate, a pheromone to disrupt themating of the codling moth, grew from 4,633 to24,710 acres of apple and pear orchards in thewestern United States (259). Adoption of theseprograms occurred because pest resistance madeconventional pesticides marginally or completelyineffective (411).

The most successful use of the sterile insecttechnique has been in the program to eradicatethe screwworm, which eats the flesh of livestockand deer. Releases of sterile male screwworms inthe United States began in 1951 and the pest waseliminated from the country by 1982 (see box 5-2 in chapter 5). Continuing programs have eradi-cated the pest from the north of Central Americaas well. An ongoing program in place in Califor-nia against the Mediterranean fruit fly (Ceratituscapitata) has not eliminated the pest: The fly per-sisted in the Los Angeles basin in 1994 despitereleases of 14 billion sterile flies in 1993 (411).Whether this result represents a failure of thesterile insect technique or repeated introductionof the pest is unclear.

Various BBTs (natural enemies, microbialpesticides, behavior-modifying chemicals) areunder investigation for control of pests in grain

storage facilities (344). Cleanit AG of Switzer-land is developing a product based on a phero-mone that repels mice to reduce rodent damage(115). None are yet in use.

Virtually no BBTs are in use today for controlof weeds in arable agriculture.7 Classical biolog-ical control has been attempted for four weedswithout success to date. Potential microbial pes-ticides have been explored for 23 crop weeds,and effective agents found for 13. Two wereeventually marketed: Collego was registered in1982 for control of northern joint vetch(Aeschynomene virginica) and DeVine was regis-tered in 1981 for control of citrus strangler vine(Morrenia odorata) in Florida citrus groves.These products were later withdrawn from com-mercial sale because they did not generate largeenough markets (see box 3-1 earlier in this chap-ter). The problem with DeVine was that it provedtoo effective, persisting in the field and givinggood weed control for more than three to fouryears at some sites (420,49). Small markets alsoresulted because each microbial product con-trolled only a single weed, whereas farmers usu-ally have to deal with many weeds at once. Thisyear, the producer of DeVine, Abbott Laborato-ries, cooperated with EPA to bring the productback on the market (49).

Conventional pesticides have never been ableto control some serious plant diseases caused byviruses and bacteria (138). Microbial productsand systems for control of plant diseases are justnow becoming commercially available (138).These microbes may suppress disease-causingmicrobes by producing antibiotics or other injuri-ous compounds, by competing with them fornutrients or other essential resources, or byinducing resistance to the disease in the hostplant. The extent to which the new microbialapproaches will be adopted and the level of con-trol they will provide are uncertain. The best-documented agricultural use of a BBT against aplant pathogen is for crown gall disease—atumor-producing disease caused by bacteria

7 A number have, however, been successful against weeds on uncultivated lands, as the next section describes.

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Chapter 3 The Technologies | 49

(Agrobacterium spp.) and affecting crops such asgrapes. No pesticides work against this disease(138). Strains of a related species (A. radio-bacter) suppress the disease, but each strainworks only against certain disease strains. Twomicrobial pesticides for crown gall are sold in theUnited States, Galltrol by the AgBioChem Com-pany and Norbac 84C by the NorTel Lab, withannual sales exceeding $100,000 (138).

In 1994 at least three new microbial productsthat enhance plant growth, in part by suppressingroot-dwelling bacteria, came on the market:Kodiak, Epic, and Quantum 4000 from theGustafson Company (138). These seed treat-ments, which colonize growing roots once seedsgerminate, are used in combination with chemi-cal fungicides. Sales in 1994 were for seeds suf-ficient for planting three million to five millionacres of cotton, peanuts, and beans; this figure isexpected to expand to 20 to 30 million acres bythe year 2000 (138). The first commercial prod-ucts for control of postharvest plant disease(which blemishes and causes rot on harvestedcrops) are just now coming on the market also.Bio-Save 10 and 11 (products based on the bac-terium Pseudomonas syringae from EcoScienceCorporation) and Aspire (product based on theyeast Candida oleophila from Ecogen) becameavailable in 1995 for control of major posthar-vest diseases of apple, pear, and citrus (161).

Disease-suppressive soils and compostsreduce crop diseases, it is thought, through theaction of bacteria, fungi, or other microbes thatdwell in these materials. Suppressive soils occurnaturally in some areas or can be created by spe-cific farming practices. Almost all are main-tained by individual farmers, and no commercialproducts are available (138). Suppressive com-posts are widely used in horticulture but are notadvertised for their disease-suppressive charac-teristics.

Pastures, Rangelands, and ForestsPest problems in these habitats pose specialproblems. The lands generally are of lower eco-nomic value, making it difficult to justify thecosts of expensive pest control programs based

on conventional pesticides. Many forests andrangelands also encompass environmentally sen-sitive habitats, such as those adjacent to water-ways, where use of pesticides may be restrictedor prohibited. The most commonly used BBTs inthese areas are various forms of biological con-trol because of the low costs and general lack ofimpacts on nontarget organisms.

Rangelands and pastures are two of the fewareas where BBTs currently are used for weedcontrol. Classical biological control agents havebeen introduced against 40 U.S. weeds. Cur-rently the approach has provided some level ofsuppression for 18 weeds and excellent controlover some or most of the range of seven of thesespecies (420). The successes include musk thistle(Carduus nutans), controlled by the weevil Rhi-nocyllus conicus, and skeletonweed (Chondrillajuncea), by Puccina chondrillina (420).

A number of programs propagate and distrib-ute weed natural enemies to enhance theireffects. The Oregon Department of Agriculture’sweed program has introduced 42 natural enemiesagainst 20 target plant pests since it began in the1970s. Program staff now collect and transferbiological control agents across weed-infestedareas to maximize the agents’ impacts. In Mon-tana, county extension agents cooperate withhigh schools and local 4-H clubs to run a similarprogram involving high school students (266). Atleast seven commercial suppliers now harvestweed biological control agents collected from thefield for sale to ranchers, land managers, and oth-ers (155).

Rangeland managers sometimes modify live-stock grazing practices to help reduce weed pop-ulations. The extent and the effectiveness of thispractice are unclear. In areas managed to con-serve native biodiversity, the use of livestock tohelp reduce weeds is sometimes undesirablebecause the cattle do not confine their impacts totarget weeds (332). Under some circumstances,however, cattle grazing can enhance plant biodi-versity. Other BBTs for weed control are not yetin use. Plant diseases have been evaluated aspotential microbial pesticides for five weeds of

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50 Biologically Based Technologies for Pest Control

In Montana students and teachers are part of a hands-on pro-gram to distribute natural enemies of noxious weeds thatdegrade rangelands,

W. Pearson, Stillwater Weed Control

pastures, rangelands, and forests, but none hasbeen developed into a commercial product (420).

Biological control has had less success againstinsect pests of forests and rangelands. Few pro-grams have been undertaken, and these have hadmixed results. The most notable success is thelarch casebearer (Coleophora laricella); intro-duction of five insect parasites from 1931through 1983 has provided significant suppres-sion of the pest throughout its North Americanrange of hundreds of millions of acres (284).8 Incontrast, the repeated expensive efforts to controlEuropean gypsy moth since 1906 by classicalbiological control have failed to produce signifi-cant suppression of the pest (table 3-1) (284).

Microbial pesticides have proved more suc-cessful than classical biological control againstthe European gypsy moth. Bt now forms the coreof the nation’s multistate gypsy moth suppres-sion program conducted by the U.S. Forest Ser-vice, the Animal and Plant Health Inspection

Service (APHIS), and state agencies (382,384).This is the single largest use of Bt in the UnitedStates, with annual applications occurring on atleast 374,000 acres (382). Isolated infestations ofEuropean gypsy moth have been eliminated byBt applications, but the microbial pesticide hasyielded more mixed results in reducing defolia-tion in high-density areas (284). The Europeangypsy moth NPV virus (Gypchek), produced bya commercial firm under contract to the ForestService, also is now applied to about 6,000 acresannually (382). The virus is costly and in limitedsupply; in 1994 the state of North Carolinaappropriated almost all of the U.S. supply tocombat the newly arrived Asian gypsy moth.9

Several additional techniques complete thecurrent BBT arsenal against European gypsymoth. Two natural enemies are sold by a privatecompany (the National Gypsy Moth Manage-ment Group) to federal, state, and municipalagencies for augmentative use at isolated infesta-tions and along the leading edges of moth out-breaks (284). In 1994, an estimated 500,000wasps (costing from $0.25 to $0.52 each) weresold, to be applied at a rate of 50 per acre.Impacts of these natural enemies are uncertain.Finally, a gypsy moth pheromone has been usedto identify and monitor the spread of gypsy mothinfestations.

Pheromone-based approaches have limitedsuccess in controlling U.S. forest pests (284).The only known successful use of mating disrup-tants has been to control the western pine shootborer, Eucosoma sonamana, in pine plantations,where pest levels were suppressed 75 percent(60). In the late 1970s and early 1980s, the masstrapping approach was used in Scandinaviaagainst the spruce bark beetle on over 4.5 millionacres of forest (310). The pest’s abundancedeclined, but it is unclear whether the pheromone

8 However, according to some scientists, the success of the larch casebearer program is impossible to prove. Too little monitoring ‘as

conducted to establish a clear cause and effect relationship between the biological control releases and the suppression of the pest (203A).Proving this type of causality in ecological systems is, however, notoriously difficult,

9 The Asian gypsy moth disperses more readily than the European gypsy moth and harms different trees. Detection of the Asian strain in.the United States not on] y caused worry about its immediate impact but also raised concern that the two strains would interbreed and give riseto an especially damaging type of gypsy moth.

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Chapter 3 The Technologies | 51

method caused the drop (39). Nevertheless, itwould be the method of choice if another pestoutbreak occurred because conventional pesti-cides are prohibited there (310).

Other pheromone techniques are under devel-opment or used occasionally, in particular,against the southern and mountain bark beetles.Pheromones that enhance beetle aggregationhave been applied to tree stands prior to cutting,causing the beetles to aggregate and then diewhen the trees are cut and removed (284). Apheromone that protects trees from attack byrepelling beetles has recently been patented andhas been tested in the National Forests in Louisi-ana, and a second is under development (284).

Grasshoppers are the only significant insectpest of rangelands to be targeted thus far byBBTs. Of the more than 300 native grasshopperspecies of western rangelands, 10 to 15 periodi-cally have population outbreaks and becomemajor pests (284). A microbial pesticide forgrasshoppers, based on the protozoan Nosemalocustae, is produced commercially by two U.S.companies: Bozeman Bio-Tech (Montana) andM&R Durango (Colorado). The current numberof acres treated with this product is very smallcompared with the number treated with chemicalpesticides (411). A product based on the fungusBeauvaria bassiana was registered by MycotechCorporation in 1995, as mentioned earlier in thischapter. Two other BBT alternatives underresearch are a fungus (Entomophaga praxibuli)and a parasitic wasp (Scelio parvicornis). Thelatter was recently denied a permit for release bythe USDA Animal and Plant Health InspectionService because of concerns about potential non-target impacts (299).

Natural Areas, Parks, and Wildlands10

Until recently, few BBTs were targeted specifi-cally at pests of natural areas and wildlands.Increasing awareness of how invasive nonindige-

10 Natural areas and wildlands are distinguished from rangelands, forests, and pastures. The latter are managed primarily for theirresource values, such as cattle grazing and timber. Natural areas and wildlands, in contrast, are managed to support native plants and animals;they include many federal and state parks, refuges, and wilderness areas.

nous (exotic) species are threatening nativebiodiversity (338), however, has led natural areamanagers begin to explore BBT options for pestcontrol—classical biological control, in particu-lar (box 3-3).

Classical biological control has particularadvantages in natural areas and wildlands (284).An established biological control agent can pro-vide indefinite control of a pest, tracking itsspread and bringing it under control at new sites.Biological control may thus be the only econom-ically feasible option for certain widespreadpests like yellow starthistle (Centaurea solstitia-lis)—a weed that displaces native vegetation anddegrades wildlife habitat on western range-lands—for which the costs of conventional pesti-cides would be exorbitant. Classical biologicalcontrol agents, if properly screened are unlikelyto have undesirable environmental impacts (seechapter 4, however, for a discussion of potentialimpacts and screening methods).

Natural area managers have not wholeheart-edly embraced biological control (284). The pri-mary concern is whether impacts of the controlagent are confined to the pest or also affect otherorganisms. Far more so than in agriculture, con-cerns of natural area managers extend to a widevariety of organisms, and many see potentialnontarget impacts as a serious liability. For simi-lar reasons, natural area managers view use ofbiological control for native pest species with agood deal of alarm. Certain species may be pestsin some locales but integral components ofnative ecosystems in others. Poison ivy (Toxico-dendron radicans), for example, is an importantsource of wildlife forage. Moreover, native pestsare far more likely to have nonpest relatives inthis country that would be especially vulnerableto their biological control agents (332).

Despite these concerns, natural area managershave begun to proceed cautiously with classicalbiological control programs. Most have been

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52 | Biologically Based Technologies for Pest Control

conducted by federal, state, and local agencies. Ahandful of related projects have taken place inprivate reserves; one was recently approved bythe Nature Conservancy (284). Most of theseprograms have piggybacked on better-supportedprograms aimed at pests of agriculture, range-lands, commercial forests, urban lands, and navi-gational waterways, because many of these pests

also affect natural areas and wildlands. Examplesinclude the gypsy moth, numerous rangelandweeds, salt cedar (Tamarix spp.), and hydrilla (aweed that blocks waterways).

Classical biological control programs inHawaii have targeted at least one weed invadingnature reserve forests, banana polka (Passifloramollissima), using introduced plant diseases

BOX 3-3: How Conservationists are Turning to Biological Control to Help Save Biodiversity

The imported red fire ant (Solenopsis invicta) first entered the United States from South America in the1930s. It has since spread to 250 million acres from Texas to Virginia. Conventional pesticides haveproved ineffective at controlling the pest, despite expenditures of more than $200 million. Some expertsbelieve that the mass sprayings in the 1950s and 1960s may even have hastened its spread by weaken-ing native ant species that could compete with the fire ant.

The red fire ant is well known for its aggressive stings to humans that can cause allergic reactions andeven death in sensitive individuals. It has similar effects on domesticated animals. Texas veterinariansrank fire ants as a serious threat to animal health and report that annual costs to treat stung animalsamount to $750,000 in that state alone.

Now conservation biologists across the country are warning that the red fire ant may have direimpacts on biodiversity as well. In places, some scientists believe that it has reduced native insect spe-cies by as much as 40 percent. Seed-harvesting ants have disappeared in many areas of Texas, alongwith certain lady beetles, spiders, scorpions, and other arthropods. Studies of Texas pigmy mice showalterations in the mice’s behavior and ecology where the red fire ants are present. Survival of white-taileddeer fawns is reduced by half where the ants occur: Facial stings sometimes blind or kill fawns. Declinesin one endangered grassland bird (the loggerhead shrike) correlate directly with the presence of fireants. And the evidence suggests that several other migratory grassland birds may be similarly affected.

According to E.O. Wilson, a well-known biodiversity and ant expert from Harvard University, control ofthe fire ants may be necessary to avert a small-scale catastrophe for insect biodiversity in the South.Such concerns have prompted scientists in Texas and Utah to search for biological control agents to useagainst red fire ants. Several flies (Pseudacteon spp.) that parasitize the ants are currently under study.Instead of providing direct control of the fire ant, researchers expect the parasites to reduce the fire ant’sability to compete with native ants. Several other biological strategies are being considered, such astreating the ant colonies with the species’ own pheromones to halt reproduction. Scientists in Florida alsoare investigating ways of baiting fire ants into carrying the pathogenic fungus Beauveria bassiana back totheir nests.

The imported red fire ant is but one of several pests now being targeted for control because of theirimpacts on biodiversity. Purple loosestrife (Lythrum salicaria) and melaleuca (also known as the paper-bark tree, Melaleuca quinquenervia) are other prominent examples. Both are wetland weeds that dis-place native plants and degrade wildlife habitats.

SOURCES: J. Grisham, “Attack of the Fire Ant: Scientists Hope New Methods of Biocontrol Can Stop the Advance of this ImportedPest,” BioScience 44(9):587-590, October 1994; C.C. Mann, “Fire Ants Parlay Their Queens Into a Threat to Biodiversity,” Science263:1560-1561, March 18, 1994; J. Randall and M. Pitcairn, Exotic Species Program, The Nature Conservancy, Galt, CA and theBiological Control Program, California Department of Food and Agriculture, Sacramento, CA, “Biologically Based TechnologiesFor Pest Control in Natural Areas and Other Wildlands,” unpublished contractor report prepared for the Office of TechnologyAssessment, U.S. Congress, Washington, DC, November 1994.

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Chapter 3 The Technologies | 53

(420). Only a few pests of natural areas in NorthAmerica that have few or no impacts elsewhere,such as purple loosestrife (Lythrum salicaria)and melaleuca (Melaleuca quinquenervia), arecurrently the subjects of ongoing classical bio-logical control programs by federal and stateagencies (109,284). Natural area managers gen-erally hold little hope that many new BBTs willbe developed specifically for these areas (284).

Urban and Suburban EnvironmentsPest control takes place in intimate associationwith human populations in urban and suburbanenvironments. Consequently, potential exposureto pesticidal products is high. Markets havedeveloped for BBT products, in part because oftheir appeal to consumers who wish to avoiddirect contact with conventional pesticides. BBTapproaches lacking a commercial product havebeen exploited only rarely in urban and suburbanenvironments because research by academic andgovernment scientists has generally been lack-ing. For example, classical biological control hasbeen used against few pests of turfgrass andshade trees (60).

Various bait-type products are sold for controlof structural pests (including cockroaches andtermites) that infest houses and other buildings.Control of these pests is a multibillion dollarindustry in the United States. A new microbialproduct that came on the market in 1993 is calledBio-Path. It consists of a bait station that harborsfungus spores (Metarrhizum anisolpliae)designed to infect entering roaches, which thenspread the pathogen to other individuals (60).

Use of natural enemies and microbial pesti-cides around food preparation and storage areasis another recent development. At least one natu-ral enemy is now sold commercially for use infood storage facilities—the parasitic wasp Bra-con hebetor, for control of Indianmeal moth(Plodia interpunctella) in peanuts. Some contro-versy has surrounded attempts to expand usesinto food preparation areas. The small company

Praxis met resistance from state and federal regu-lators when it began selling pest control pro-grams based on parasitic wasps and nematodepesticides for use in cafeterias and restaurants(70) (see box 4-8 in chapter 4).

Natural enemies have found application ininteriorscapes (interior plantings) of shoppingmalls, hotels, office buildings, zoos, and muse-ums (320). One attraction is that they reduce lia-bility considerations related to public exposure topesticides. An example is the “Tropical Discov-ery” display of the Denver Zoological Garden,where establishment of natural enemies has cutthe costs of pest control in half and reducedpotential impacts of pesticides on animals in theexhibit. Use of natural enemies as an overallstrategy in interiorscapes can be hampered ifnone are available for certain pests like brownsoft scale (Coccus hesperidum),11 necessitatinguse of insecticides that may damage natural ene-mies where such pests are present (60).

Homeowners seeking to deal with turfgrasspests make up about 35 percent of the U.S. mar-ket for nematode-based pesticides (411). Thegrass seed industry now sells several varietiescontaining endophytes that enhance pest resis-tance. Sales of turfgrasses with endophytes areexpected to grow because of increasing con-sumer demand for “environmentally friendlyturfgrass” (306). Consequently, the developmentof techniques to transfer endophytes to new grassspecies is an especially active area of research inthe turfgrass industry.

Nevertheless, interest in BBTs by the lawnand landscape industry has been patchy. One1990 survey of 17 commercial arborist firmsfound that 11 used Bt, nine used pheromonetraps, and three made augmentative releases ofnatural enemies (248). An important problem hasbeen inconsistent product performance (seedescription of milky spore in box 3-1, earlier inthis chapter). Another is that microbial pesticidescompete directly with other “natural” pesticides.For example, Bt-based pesticides active against

11 A natural enemy for control of brown soft scale is expected to become commercially available in late 1995 (410A).

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leaf beetles came on the market for shade treecare in the mid-1980s. Short field persistence,the need for careful timing of application, andhigh prices resulted in market failure for theseproducts, especially when botanically derivedneem pesticides, which appeared in the early1990s, proved to be more effective alternatives(60).

Another reason for the relatively low interestin BBTs among landscape companies is theindustry’s increased emphasis on ensuring thatplants are healthy by meeting the plant’s envi-ronmental requirements. Recommended prac-tices include promoting populations of beneficialmicroorganisms (i.e., conserving them) to pre-vent plant diseases (110). BBT products are seenas an adjunct to this approach (295).

Although few classical biological control pro-grams have been targeted toward insect pests ofurban and suburban environments, an importantrecent exception is the ash whitefly (Siphoninusphillyreae). Control of this pest by an importedwasp parasite (Encarsia inaron) has proved soeffective that the whitefly is no longer a majorpest in California; the biological control agenthas now been released to suppress other infesta-tions of ash whitefly in Arizona and Nevada (60).

Three microbial products are available forcontrol of plant pathogens. Urban and suburbanapplications of Galltrol are limited to protectingnursery materials, specifically roses and otherornamental plants, for sale to consumers (60).Bio-Trek and T-22G are formulations of Tricho-derma harzianum that became available in 1995for use as a greenhouse potting soil amendmentand a golf course inoculant. No BBTs currentlyaddress urban and suburban weed problems, butproducts for broadleaf weed (i.e., dandelion)control are under development (60,233).

Aquatic EnvironmentsMost applications of BBTs to aquatic pests thusfar have been for control of weeds that block

navigational waterways and of the larvae of mos-quitoes that pose a risk to human health. Themethod of choice has often been introduction offish predators.

The grass carp (Ctenopharyngodon idella), afish that consumes most aquatic plants, has beenstocked in more than 35 states for control ofaquatic weeds (191). The fish clear plants fromwaterways so effectively that habitats of otherfishes, invertebrates, and waterfowl may bedestroyed. At least 21 states now require releasedgrass carp to be sterile to limit their impacts,although another 10 states still allow uses of nor-mal reproductive fish.12 Certain other fishes,such as blue and red tilapia (Tilapia aurea and T.zillii ), also have been introduced to a lesserextent for aquatic weed control (191).

Classical biological control programs haveyielded some control for three important aquaticweeds—alligatorweed (Alternanthera philoxeroi-des), water hyacinth (Eichhornia crassipes), andwater lettuce (Pistia stratiotes) (191). Fungi thatcould be developed into microbial pesticideshave been identified for two aquatic weeds,water hyacinth and Eurasian water milfoil(Myriophyllum spicatum), but neither has beendeveloped commercially (420).

Mosquitoes spend the earliest part of theirlives as swimming larvae and are the most signif-icant insect pests in aquatic habitats. The mos-quito fish (Gambusia affinis) is the one mostcommonly used to control the pest. It is nowfree-living throughout much of the United Statesas a result of its widespread release for this pur-pose (191). Several other fishes (e.g., the flat-head minnow, Pimephales promelas, and theblue-gill sunfish, Lepomis macrochirus) havebeen put to similar use.

Certain microbial pesticides are in use orunder development for mosquito control. Astrain of Bt (specifically, Bacillus thuringiensisisraelensis or Bti) is now widely applied for con-trol of mosquitoes and blackflies. Its use is lim-

12 Sterility is accomplished by making the fish triploid, that is, having three sets of chromosomes rather than the normal complement oftwo.

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ited to upland and freshwater habitats; it is noteffective in major sites for mosquito breeding insalt marshes (134). Another microbial pesticidederived from Bacillus sphaericus also is com-mercially available for mosquito control.

Scientists have identified several fungi thatkill mosquitoes (Coelomyces spp. and Lagenid-ium spp.). A number of other invertebrates (flat-worms, nematodes, and copepod shrimp) havebeen shown experimentally to consume mosqui-toes. None has yet been put to practical use inmosquito control programs (191).

BBTs have also been applied to control inver-tebrate and fish pests. Releases of a snail compet-itor (Marisa cornuarietis) into Puerto Ricanwaterways during the 1960s greatly reduced pop-ulations of the snail Biomphalaria glabrata, acarrier of the parasitic worm that causes schisto-somiasis. Prior to the biological control program,this human disease infected approximately onemillion people in Puerto Rico. Northern pike(Esox lucius) and walleye (Stizostedion vitreum)have been used to control nuisance fishes, suchas the ruffe (Gymnocephalus cernuus) (191).

The U.S. invasion of the zebra mussel (Dreis-sena spp.) in the 1980s brought new nationalattention to the economic and environmentalhazards of nonindigenous aquatic pests (338).Scientists have begun to examine various fishesand microorganisms for biological control of thiscostly pest. Some scientists believe that BBTshave considerable potential for application toaquatic environments generally; for example,classical biological control might control theEuropean green crab (Carcinus maenas), a shell-fish predator that was recently detected near SanFrancisco and may imperil the Washington Stateoyster industry (191). The Australian govern-ment has just started a new research center—funded at $1 million annually and with a plannedstaff of five—to identify biological controlagents for nonindigenous marine pests thatthreaten fisheries or marine ecosystems (192).An important issue, should U.S. interest inaquatic uses of BBTs grow, relates to the virtuallack of federal regulation and the erratic attentionby states to deliberate introductions of aquatic

species as biological control agents (338) (seebox 4-2 in chapter 4).

❚ What’s Coming Next

New Microbes and Microbial PesticidesA wide variety of microbial pesticides are cur-rently under development. When these reach themarket they will greatly expand the repertoire ofcommercial product types. The extent to whichthese products and approaches will be adopted isuncertain. In some cases, development of newmicrobial pesticides will involve identification ofnew strains of microbes currently available. Btproducts with activity against a greater range ofpests are likely to be developed. Ecogen hasalready marketed a product (Foil) that actsagainst both caterpillar and beetle pests by com-bining the genes of two bacterial strains throughconjugation—a naturally occurring processthrough which bacteria exchange genes.

Other pesticides rapidly coming on line willbe based on types of microbes not yet in wideuse. Several commercial companies are develop-ing microbial pesticides based on fungi for insectcontrol, including EcoScience Corporation (Bio-blast for termite control); Mycotech Corporation(Mycotrol-GH for grasshopper, mormon cricketand locust control, and Mycotrol-WP for white-flies, aphids, thrips, mealybugs, and psyllids);and Troy BioSciences (Naturalis-O for use onornamentals against whiteflies, aphids and mitesand Naturalis-T for turf use, controlling molecrickets and cinch bugs). Commercial develop-ment is well advanced for microbial products(based on bacteria Pseudomonas fluorescens andErwinia herbicola) to control fire blight, a verydestructive disease of apples and pears caused bythe bacterium Erwinia amylovora, with salesexpected to begin in 1995 (138,161). SoilGard, aproduct based on the fungus Gliocladium virens,for damping-off diseases of seeds and seedlingsin greenhouse production of vegetables and orna-mental bedding plants, is now in the final phasesof development by W.R. Grace Co. (138).

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CONTROL 22 x 10’ 32 x 10' 54 x IdL-59-66 CFU ML

COLD STORAGE 30 DAYSPEXPANSUM

Development of microbial pesticides for controlling the dis-eases that cause harvested produce to spoil is an active area ofresearch. The unblemished fruit have been treated with a micro-organism that prevents the pears from rotting.

Agricultural Research Service, USDA

A number of other microbe-based approachesand products are being researched but are not yetnear product development or field use. Scientistspredict that more insect viruses (many alreadyidentified) will become an attractive option asresistance to conventional pesticides emerges incommon pests. Microbial approaches to Euro-pean gypsy moth control based on protozoans’s

and fungi are under investigation as ways to helpcombat this tenacious pest (41 1,284). Consider-able research interest continues to center on con-trol of common plant diseases such as take-alland root rot diseases of wheat (1 38).

Novel delivery systems for microbial controlagents are also under development. One involvesputting microbial pesticides that work againstplant pathogens into beehives so that bees trans-port the microbes to the plant (138). Another isbased on modifying the algae food of mosquitolarvae to contain a mosquito poison (85).

Genetic Manipulations of BBTs and PestsBBTs are based on living organisms and theirproducts. Consequently, it is not surprising thatefforts to improve BBTs focus to a significant

degree on genetic modifications through breed-ing, selection, genetic engineering, 14 and othertechniques.

Most microbial pesticides now on the marketwere developed through the selection of effica-cious microbe strains. Many companies involvedin the development of microbial pesticides arenow attempting to alter such features as kill rate,field persistence, environmental range, and thenumber of target pests through genetic engineer-ing. Mycogen has recently put four products onthe market all based on Cellcap, its geneticallyengineered Bt encapsulated within a Pseudomo-nas fluorescens bacterium (42). Ecogen broughta genetically engineered Bt on the market in1995 called Raven (167). Sandoz Corporationrecently conducted field tests of genetically engi-neered Bt in California and elsewhere in thecountry. Efforts to genetically engineer microbialpesticides are widespread, and they involve mostpotential product types, including those affectinginsects (Bt, NPV viruses, and nematodes),weeds, and plant pathogens (138,191,41 1,420).

The scientific community is divided over thedesirability of this approach. Some researchersbelieve that improvement through genetic modi-fication will be essential for certain types ofmicrobial pesticides to become widely adopted.Others express concern that, as microbial pesti-cides become more equivalent to conventionalpesticides, scientists will engineer out the verycharacteristics of target specificity and short fieldpersistence that make Bt and other current micro-bial pesticides relatively benign (41 1).

Similar questions divide scientists over ongo-ing attempts to genetically modify natural ene-mies. In this research, breeding, selection, orgenetic engineering is being used to enhance thecompatibility of natural enemies with conven-tional pesticides (152). A less precise version ofthis approach is already practiced in the naturalenemy industry; a number of companies collect

13 Protozoans are certain single-celled organisms whose internal structure is more like that of cells from higher organisms than bacteria.14 Genetic engineering refers to recently developed techniques through which genes are isolated in a laboratory, manipulated, and then

inserted stably into another organism. Offspring of the recipient contain the new genes.

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their breeding stocks from areas where pesticideuse is high and the natural enemies are morelikely to have developed some resistance tochemicals. Some entomologists worry, however,that pesticide-resistant natural enemies will dis-courage the development of biological controlmethods for other pests (411).

Genetic modification of the pest instead of itscontrol agent has long been practiced in the ster-ile insect approach. Attempts to extend thismethod to other types of organisms, such as thesea lamprey (Petromyzon marinus)—a parasiticfish that impairs the Great Lakes sport fishery—have been studied but have not yet proved effec-tive (191).

Another approach to genetically modifyingpests, by producing pest strains lacking noxiousqualities, was first suggested 25 years ago. It iscurrently under study for a number of medicallyimportant pests. Efforts are under way to creategenetically engineered mosquitoes that cannotcarry and transmit to humans the parasite thatcauses malaria (4). Similar approaches have triedto make snail vectors of human diseases unableto carry human parasites; as yet, thoseapproaches have been unsuccessful because thegenetically altered strains are less viable (191).

Genetic modification of the pest is also beingapplied to plant diseases. Researchers are tryingto develop less damaging (“hypovirulent”)strains of the microbes that cause chestnut blight(Endothia parasitica, a fungus) and Dutch elmdisease (Ceratocystis ulmi, another fungus)—diseases responsible for the near elimination ofnative chestnut (Castanea sativa) and elm trees(Ulmus spp.) from the American landscape(60,284). The method has already proved suc-cessful in Italy where, following inoculation ofchestnut trees, a hypovirulent strain spread tobecome the most common form of the chestnutblight fungus, and chestnut trees are again beingharvested commercially.

Although outside the scope of this assessment(see box 2-5 in chapter 2), among the mostwidely discussed technologies coming on line isgenetic engineering of plants for enhanced resis-tance to pests and pathogens. A number of crop

plants, including tomatoes, potatoes, and cottonhave been altered to express Bt toxins. Corn seedthat has been genetically engineered to producethe Bt toxin has just been approved for commer-cial sale. Widespread use of such crop cultivarsmight increase the speed with which pestsbecome resistant to Bt (see chapter 4). The intro-duction of virus coat protein genes into plants toenhance their resistance to certain viral diseasesis being explored, with a new virus-resistantsquash expected to become commercially avail-able soon. Questions remain regarding the possi-bility that introduced virus genes mightrecombine with other viruses attacking the plantand form new, and possibly more damaging,viral strains.

Other New ToolsPractical applications of techniques discussed inthis section lie at least a decade in the future.Allochemicals, for example, are chemicals thatplants under attack by a predator emit and thatattract the predator’s natural enemies. Thesechemicals might be used to attract and concen-trate natural enemies or to trap or deflect pests.Secretion of allochemicals is one of severalimportant plant attributes that may have beenweakened in the development of agricultural cul-tivars because the role of the chemicals in bio-logical control was not well understood (411).

Scientists also are beginning to understandhow plants’ own sophisticated defense mecha-nisms might be exploited to suppress plant dis-eases. These defense mechanisms can beenhanced by exposing the plant or its seeds tocertain microbes or chemicals. “Induced resis-tance” has been demonstrated in at least 25crops; commercial products based on thisapproach are under development (233,138).Development of methods to transfer endophytesinto plants (including agricultural crops) inwhich they do not naturally occur is anothermethod under study to increase disease and pestresistance. Plants can also be “cross-protected”by infecting them with a milder strain of a dis-ease agent; this process has been demonstrated invarious crop plants. It is now being used on a

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pilot basis in Florida for control of diseasescaused by the citrus tisteza virus which affects 25million to 30 million sour orange trees in theUnited States. The same method is being usedcommercially in South Africa, Brazil, and Aus-tralia. Large scale use of cross protection, how-ever, lies well into the future because significanttechnical problems remain; for example, thesame mild strain that gives protection to one cropmay produce disease symptoms in another (138).

OBSTACLES TO EXPANDED USE OF BBTSExplanations of why BBTs are not in wider useusually center on a number of commonlyacknowledged obstacles. Certain technical obsta-cles reflect hard limits to what the technologiescan do or how they are produced and delivered inthe field. They can be addressed only by ade-quate adjustment of the research agenda and byprovision of mechanisms to ensure that researchresults become available for field applications(table 3-2). The greater emphasis, however, evenamong technical experts, is usually on the social,economic, and institutional factors that affect thedevelopment and adoption of BBTs, and theserequire policy solutions.

❚ Integration of BBTs into Pest Control SystemsBBTs almost always need to be integrated intoan overall system for pest management—usuallyan integrated pest management system—thatincorporates a variety of tools and techniques toprevent pest problems or to control outbreakswhen they occur. While IPM adoption in theUnited States is growing, it is by no means thedominant approach to pest control. This lack ofwell-developed IPM systems significantly limitsthe use of BBTs.

Even the IPM systems in existence today donot always do a good job of incorporating BBTs.Developing integrated programs that includeBBTs requires a sustained commitment ofresources and expertise (e.g., ref. 133). BBTsmust also compete directly with other methods

that often provide a superior level of control (seebox 3-2, earlier in this chapter). The research onmicrobial pesticides to bring performance morein line with conventional pesticides is not sur-prising in this light (149).

Moreover, BBTs require a level and type ofknowledge not yet acquired by many pest controlpractitioners or even by people who advise users,such as members of the Cooperative ExtensionService or private pest control consultants.Appropriate information on BBTs may thus belacking, even where there are users who wouldbe willing to experiment with these approaches(see chapter 5). The proliferation of Internet sitescontaining information on pest management mayeventually provide easier access to informationresources for those having the right equipmentand software. (See appendix 3-A immediatelyfollowing this chapter for current list of relevantsites.) At present, however, tracking down cor-rect information is not straightforward or easy;information on the Internet varies in quality andlacks a centralized organization or means ofaccess.

Another problem is that, to a large extent, thefield of biological control developed separatelyfrom that of IPM (319). This separation posesreal difficulties for the full incorporation of bio-logical control into IPM systems. Coordinationwith other control methods is not always anexplicit goal of U.S. research on biological con-trol. Some experts in biological control believe itshould never be integrated in IPM programs withconventional pesticides. A symptom of this disci-plinary separation is the recent failure to includerepresentation of APHIS’s National BiologicalControl Institute in USDA’s current initiative onIPM.

Compatibility with conventional pesticidesmight be an important determinant of how effec-tively BBTs can be combined into certain typesof IPM programs. Pheromones and many micro-bial pesticides can be used alongside conven-tional pesticides (175). Certain microbialpesticides are actually more effective when usedin conjunction with chemicals. Biological controlposes a different challenge, though. Natural ene-

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mies sold for augmentative uses are highly sensi-tive to pesticides; suppliers often recommendwaiting several weeks following pesticide appli-cation before releasing natural enemies.

If pesticides could be selected to minimizetheir impacts on natural enemies, it might be eas-

ier to incorporate the various forms of biologicalcontrol into IPM systems. One problem is thatsuch information is not widely available. BrianCroft, a professor at Oregon State University, hasbeen accumulating a related database for severalyears, but support for the project has been erratic

TABLE 3-2: Priority Research Needs Identified by OTA’s Contractors

Research Need Potential Resulting Benefit

Develop basic information on the biology and ecology of pest systems, including the taxonomy and systematics of pests and control agents

Enable development of more predictive approach to the identification of possible control agents for specific pestsEnable development of more sophisticated approaches to biologically based pest management

Improve methods to test for nontarget effects of BBTs Minimize environmental hazards

Develop application techniques for existing and new BBTs

Enable better use of BBTs under field conditions

Identify new and more efficacious microbes Improve performance of microbial pesticides

Integrate BBTs into IPM systems Increase use of BBTs in situations where they will be effective

Improve formulation, production, packaging, and delivery techniques for microbial pesticides (including in vitroa production methods for viral pesticides)

Reduce costs and improve performance of microbial pesticides

Improve production, packaging, and delivery techniques for natural enemies (including in vitroa production methods)

Reduce costs and improve performance of natural enemies

Improve formulations for delivery of pheromones Improve performance of pheromones

Monitor classical biological control agents after release Improve ability to predict which agents will workImprove documentation of actual efficacy of biological control

Identify BBTs to address pests of natural areas, aquatic habitats, and urban/suburban environments

Address current pest control needsTransfer existing technologies to new applications

a In vitro refers to production outside a living organism. Current production techniques for most viral pesticides and natural enemies are in vivo,that is, the agent is produced on or inside a living organism.

SOURCES: Compiled by Office of Technology Assessment, U.S. Congress, 1995, from G. E. Harman and C.K. Hayes, Departments of Horticul-tural Sciences and Plant Pathology, Cornell University, Ithaca, NY, “Biologically Based Technologies For Pest Control: Pathogens That Are Pestsof Agriculture,” unpublished contractor report prepared for the Office of Technology Assessment, U.S. Congress, Washington, DC, October1994; A. Kuris, Department of Biological Sciences and Marine Science Institute, University of California, Santa Barbara, CA, “A Review of Bio-logically Based Technologies For Pest Control in Aquatic Habitats,” unpublished contractor report prepared for the Office of TechnologyAssessment, U.S. Congress, Washington, DC, October, 1994; J. Randall and M. Pitcairn, Exotic Species Program, The Nature Conservancy,Galt, CA and the Biological Control Program, California Department of Food and Agriculture, Sacramento, CA, “Biologically Based Technolo-gies for Pest Control in Natural Areas and Other Wildlands,” unpublished contractor report prepared for the Office of Technology Assessment,U.S. Congress, Washington, DC, November 1994; R. Van Driesche et al., Department of Entomology, Univeristy of Massachusetts, Amherst,MA, “Report on Biological Control of Invertebrate Pests of Forestry and Agriculture,” unpublished contractor report prepared for the Office ofTechnology Assessment, U.S. Congress, Washington, D.C., December 1994; A.K. Watson, Department of Plant Science, McGill University,Quebec, Canada, “Biologically Based Technologies for Pest Control: Agricultural Weeds,” unpublished contractor report prepared for the Officeof Technology Assessment, U.S. Congress, Washington, DC, November 1994.

NOTE: This list was derived by comparing and compiling suggested research priorities from background reports prepared by OTA’s contrac-tors on the application of BBTs to various categories of pests. A few additions were made by other experts.

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and no government agency has attempted tomake the information easily accessible to farm-ers (61,62). Similar data are required for registra-tion of pesticides in Germany (106) (see chapter4). The impending loss of minor use pesticidesmay cause some chemicals that are more com-patible with natural enemies to become unavail-able.

Moreover, it is unclear whether certainBBTs—biological control, sterile insectapproaches, and mating disruption—will offertheir maximum effects as part of farm-based IPMprograms. Some scientists from the USDA Agri-cultural Research Service believe that certainBBTs work best as part of areawide pest man-agement programs (box 3-4).

BOX 3-4: The Areawide Pest Management Concept

Areawide pest management is an approach that has been widely promoted by E.F. Knipling—former

director of the Agricultural Research Service’s Insect Pest Management Program and well-known origina-tor of the sterile insect approach that has been so successful in screwworm (Cochliomyia hominivorax)

eradication.

The concept underlying this approach is that biological methods, specifically, biological control andsterile insect releases, will be most effective if used on a larger geographical scale than just the single

farm. Such large-scale programs reduce residual pest populations off the farm and address the tendencyof pests and their control agents to move from site to site.

According to Knipling:

The foundation of most current integrated pest management programs (IPM) is reliance on natural control

factors to the maximum extent before resorting to the application of insecticides. While, on a short-term basis,

this can go a long way towards reducing the amount of insecticides used, it does not in any way lessen the

dependence of individual growers on insecticides as the major component in the integrated system.... We know

from experience that natural controls—as vital as they are—do not provide the protection needed for a wide

range of persistent insect pests....

Knipling asserts that classical and augmentative biological control will rarely provide the level of con-

trol desired by farmers unless the density of the biological control agent is boosted through mass propa-gation and repeated releases. He believes that several important pests are good candidates for the

method, including boll weevil (Anthonomus grandis), European corn borer (Ostrinia nubilalis), and tropi-cal fruit flies. Knipling’s approach remains largely untried to date because of the high costs of even pilot

trials of projects at such a large scale.

Evidence from pink bollworm (Pectinophora gossypiella) management in Arizona, however, has

shown that areawide uses of pheromones can be quite effective. USDA is currently considering areawideprograms based on pheromones for codling moth (Cydia pomenella) and corn rootworm (Diabroticaspp.) as part of its ongoing IPM Initiative.

SOURCES: E.F. Knipling, former Director of Insect Pest Management Program, Agricultural Research Service, U.S. Department ofAgriculture, MD, personal communication, June 5, 1995; U.S. Department of Agriculture, Agricultural Research Service, Princi-ples of Insect Parasitism Analyzed From New Perspectives, E.F. Knipling, AHN 693 (Washington, DC: U.S. Government PrintingOffice, 1992).

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❚ Understanding the Ecologyof Pest SystemsRepeatedly, scientists have called for increasedstudy of the biology and ecology of pest systems.Such information underlies the development ofall biologically based pest management, but ourcurrent level of knowledge is not high. Increasedunderstanding of pests—how they spread andwhat causes their populations to rise and fall—would allow better targeting of BBTs to thepests’ vulnerabilities. More knowledge of theecological relationships between pests and theircontrol agents might enable scientists to betterpredict what controls are likely to work and forwhat specific pests. As practiced today, the iden-tification of new microbial pesticides and biolog-ical control agents is usually based on trial anderror, making progress slow.

For example, researchers cannot with greatconfidence identify in advance the specific bio-logical control agent, or even in many cases thetype of control agent, that will actually suppress agiven pest. Instead, scientists usually identify anumber of potential agents, release them, andthen see which ones, if any, provide some levelof pest suppression. Monitoring and evaluationof the impacts of previous biological control pro-grams would help in the development of predic-tive models to sharpen the focus in classicalbiological control programs and would improveassessments of the potential ecological risks ofbiological control releases (see chapter 4). But achronic lack of such followup studies in theUnited States means that little such informationis now being generated through current pro-grams. The programs of other countries, such asAustralia and South Africa, do a far better job inthis area (76).

Better understanding of the ecology of pestsystems will not, on its own, ensure greater suc-cess. Existing theory is not always well incorpo-rated into the development of biological controlprograms. Moreover, theory only goes so far.The idiosyncrasies of each pest problem will stillrequire case-by-case development of solutions.

❚ Technical Needs and Economic Issues Related to Larger Scale UseLarger-scale use of BBTs would entail large-scale production, distribution, and application ofnatural enemies, sterile insects, and microbialpesticides. The necessary technologies are notwell developed in many cases. Mass productionand application of natural enemies, for example,would be expensive and difficult using currenttechniques (173). Government agencies andcommercial companies currently rear most natu-ral enemies on living material (in vivo produc-tion). The techniques are labor intensive andexpensive. A few of the natural enemies nowsold commercially, such as convergent lady bee-tles (Hippodamia convergens) and certain natu-ral enemies of rangeland weeds, are collectedfrom free-living populations. Such collectionposes other problems related to effects on thewild populations and the ethics of allowing pri-vate companies to remove from public lands nat-ural enemies that have been placed there atpublic expense (see chapter 4) (185).

As living organisms, natural enemies have ashort shelf life and require great care in handling(e.g., a temperature-controlled environment).Basic information about the timing, numbers,and methods of application for natural enemies isscarce. All of these limitations contribute to thecurrent problems with many natural enemies—they are difficult to use, costly, and performerratically in the field. The development of artifi-cial media for rearing natural enemies (in vitroproduction) would streamline and probablygreatly decrease the cost of production. Betterpackaging and handling methods, as well as bet-ter information on application rates and tech-niques, could improve the consistency andperformance of natural enemies. The same tech-nologies could be applied to the production ofsome types of sterile insects for mass release andcould reduce the cost of such programs.

Problems with production and packaging tech-niques also characterize microbial pesticides.Crossover of fermentation techniques from thepharmaceutical industry has contributed greatly

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to the development of production capabilities forcertain microbial pesticides, including Bt andsome fungus-based products. Viruses, however,are still produced in live hosts. This labor-inten-sive approach has made them so expensive thatonly one is widely used in the United States(European gypsy moth NPV virus), whereas anumber of other NPV viruses are extensivelyapplied in other parts of the world where labor ischeaper (411). Industry representatives generallyagree on the need for the development of cost-effective methods of production and storage/packaging techniques to enhance product shelflife and to improve quality control and perfor-mance (149,113).

A major problem is that very little expertise orfunding exists in the public sector for developingproduction methods for natural enemy andmicrobial pesticide production (138). Similarly,the development of formulations for microbialpesticides and pheromones is typically not wellfunded. Nor are most scientists, universities, orgovernment research agencies usually willing toparticipate in research on such practical matters(138). Such research reaps few rewards in thescientific community. The restrictions on opencommunication imposed by the proprietarynature of the work may further hinder progress(327A).

Past efforts in universities and federal researchlaboratories have usually stopped, for example,once a microbial strain is identified, with theexpectation that it will be picked up by the pri-vate sector. But this halt is premature. In thecomprehensive cost accounting that companiesmust do before investing in a product, a numberof variables are important—direct R&D costs,costs of production, waste volume generated andcosts of disposal, market size, product profitabil-ity, and others. Seemingly counter-intuitive deci-sions by companies not to invest in a technology

become logical when the total cost equation isexamined (149).

Poorly developed production, packaging, andapplication technologies tend to drive up costs ofBBTs, and drive down field performance. Theoverall result is to reduce the competitiveness ofBBTs with other available methods of pest con-trol. Most end up relegated to niche marketswhere overall expected sales are small. SomeBBTs would generate only small markets underthe best of circumstances because they addressone or only a few pests. Anticipated small mar-kets can doom BBTs where the start-up develop-ment costs are high, because the market size maynot justify investment by the private sector.According to weed scientists, there are numerous“orphaned” microbial pesticides that would beeffective against weeds, but the small marketdoes not warrant the development costs (420).

IMPROVING THE ODDS OF FUTURE SUCCESSThe obstacles just described reflect difficulties indeveloping BBTs and in moving existing BBTsinto practical use. They occur at several keypoints in the research, development, and imple-mentation of BBTs (figure 3-3). OTA’s list is notnew. Similar issues have been raised many timesover the past 18 years (box 3-5), typically duringworkshops and meetings of scientific experts, themajor goal of which has been to set substantiveaspects of the research agenda. Still, numerousissues pertaining more to institutional function-ing than to the science of BBTs remain unad-dressed. The chapters that follow focus on theseinstitutional problems as well as more technicalconsiderations. Each identifies major issues andprovides options that might help resolve theseproblems in the future.

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In 1978 a special study team coordinated by USDA’s Office of Environmental Quality Activities issued

the report Biological Agents for Pest Control: Status and Prospects. Most of the report’s major conclu-

sions are as true today as they were 17 years ago. According to the report:

Pest control is an acceptable and necessary part of modern agriculture and forestry, and is required for

the protection of public health and welfare. However, some of the methods used during the past threedecades have produced some undesirable side effects. Future needs for pest control can be expected toincrease, and, as they do, prevailing conditions and attitudes are likely to dictate an increased emphasis on

pest management systems which include the use of alternative methods such as biological controlagents.... The practical feasibility of using biological agents... has been amply demonstrated, and the basic

principles relevant to the operational aspects of the use of these agents are reasonably well understood.

The study’s major findings parallel those of OTA in this report and included the following:More research is needed to improve a priori predictions of success; to develop production, stor-age, and application techniques; and to assess the impacts of use;Large-scale implementation does not follow easily from demonstrated effectiveness on a smallscale;Information on pesticide alternatives is not easily available;Users need better technical assistance;Private enterprise needs incentives to enter this area;The regulatory structure needs to be reviewed and clarified; andMechanisms are necessary to coordinate federal and state agencies, the private and the publicsectors,

SOURCE: U.S. Department of Agriculture, Biological Agents for Pest Control: Status and Prospects, (Washington, DC: U.S. Gov-

ernment Printing Office, February 1978).

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64 Biologically Based Technologies for Pest Control

Public-Sectorimplementation

● Federal lands● National pest problems■ State pest problems

A

Public sector

TheoryMore fundamental

research

Implementationresearch

= Regulation

Private sector

Commercial production

■ Microbial pesticides■ Natural enemies● Pheromone products

Information transfer toend user

■ Extension■ Pest Control Advisors■ Public education● Education by commercial

producers■ Non-profit organizations

Private-sectorimplementation

■ Farmers■ Ranchers■ Homeowners

SOURCE: Office of Technology Assessment, 1995.

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APPENDIX 3-A: INTERNET SITES FORINFORMATION ON BIOLOGICALLY

BASED PEST CONTROL

Federal agency sites Address Description

APHIS Home Page http://www.aphis.usda.gov

Provides information on the different program areas and proposed rules of the agency.

Consolidated Farm Service Agency

http://bbskc.kcc.usda.gov/cfsa.htm

Contains a large collection of agricultural research data and provides access to various agricultural publications, some pertaining to BBTs.

CSREES Partners in Research, Education, and Extension

http://www.reeusda.gov/partners/partners.htm

Provides a list of the cooperative extension offices and land grant universities and access to their Internet sites. Currently developing a search engine for all CSREES programs.

Federally Funded Research in the United States

http://medoc.gdb.org/best/fed.fund.html

Features information on the research performed by USDA and a variety of other federally funded programs. Provides search engines.

National Biological Control Institute

http://www.aphis.usda.gov/nbci/nbci.html

Supplies information on biological control, implementation, and facilitation grant programs, and the NBCI staff, as well as access to the Biological Control News.

Pest Management Bulletin http://chppm-www.apgea.army.mil/ento/index.htm#bulletins

Offers information on pest management, some based on BBTs (a publication of the U.S. Army Center for Health Promotion and Preventive Medicine Entomology Program).

Cooperative extension sites

Cooperative Extension Information Servers

http://www.esusda.gov/partners/ces-locs.htm

Lists the information servers of the cooperative extension system by state (not all cooperative extension sites offer information on agriculture).

Cornell University College of Agriculture and Life Sciences, New York State Agricultural Extension Station

http://aruba.nysaes.cornell.edu:8000/geneva.htm

Provides a search engine for all of the current programs and research of this extension station. Allows easy access to their information on biological control.

Illinois Cooperative Extension Service, Horticulture Solution Series

http://www.ag.uiuc.edu/~robsond/solutions/hort.html

Offers solutions to a various horticultural problems, including pest control, to both homeowners and horticulturists, including some involving BBTs.

Oregon Extension Entomology Report

http://www.oes.orst.edu/entomol.htm

Lists current pests of Oregon and different control measures, including biological controls.

Integrated pest management sites

Cooperative Extension System IPM National Pest Management Materials Database

http://info.aes.purdue.edu/ipmdb.html

Lists general pest management information sources. Provides a search engine to report summaries and contacts for obtaining reports. Includes information on BBTs.

(continued)

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Federal agency sites Address Description

CRC for Tropical Pest Management Biological Control Program

http://www.ctpm.org/ Offers IPM and BBT alternatives for pest control in agriculture. Includes literature citations.

National IPM Information System @ Colorado State University- Pest Alert Bulletins

http://www.colostate.edu/Depts/IPM/news/news.html

Offers information on identification of insect pests and pest control measures, including some biological solutions. Serves both homeowners and farmers.

North Carolina State University component of the National IPM Network

http://ipm_www.ncsu.edu Provides access to various IPM newsletters (national and international) focusing on present research projects.

Entomological sites

Colorado State University Department of Entomology

http://www.colostate.edu/Depts/Entomology/ent.html

Features pictures of insect pests and their natural enemies. Provides access to entomology newsletters.

EntNet [email protected] Provides instructions for subscribing to the Internet list server created by the Entomological Society of America.

Florida Entomologist gopher://sally.fcla.ufl.edu:70/11/FlaEnt

Provides information, mainly research articles, on insect control. Some mention of BBTs.

Gypsy Moth Home Page at Virginia Polytechnic Institute and State University, Department of Entomology

http://www.gypsymoth.ento.vt.edu/Welcome.html

Provides information on gypsy moths, including control methods such as Bt.

Mississippi State University Department of Entomology

http://www.msstate.edu/Entomology/ENTPLP.html

Provides access to numerous newsletters and databases that contain information on classical and augmentative biological control methods.

Resistant Pest Management Newsletter

http://www.msstate.edu/Entomology/EntHome.html

Focuses on pesticide-resistant insect pests in Mississippi and alternative control methods, including some BBTs.

Rincon Insectaries http://www.rain.org/~sals/rincon.html

Offers information on Rincon’s natural enemy products.

Sites for farmers by farmers

Farmer to Farmer http://www.organic.com/Non.profits/F2F

Allows California farmers to communicate via this newsletter and to share success stories of biological control used against common pests.

Noah’s Ark Don’t Panic, It’s All Organic Homepage of an Organic Farmer

http://www.rain.org/~sals/my.html

Escorts user to various WWW and gopher sites helpful to organic farmers, including sites for identifying pests and control methods. Provides information on the Organic Food Law and the California Certification Standards of Organic Farming.

(continued)

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Federal agency sites Address Description

Sustainable and alternative farming sites

Alternative Farming Systems Information Center

http://www.inform.umd.edu:8080/EdRes/Topic/AgrEnv/AltFarm

Provides links to sustainable agriculture sites and documents as one of the 10 information centers at the National Agriculture Library of USDA. Supplies bibliographies, many on BBTs.

Information on Sustainable Agriculture

gopher://zeus.esusda.gov:70/11/initiatives/sustain

Supplies information on current research on sustainable agriculture and various news bulletins.

Plants and Sustainable Agriculture

http://www.envirolink.org/pubs/Plants.html

Provides access to sustainable agriculture newsletters and information sources, some containing information on BBTs.

University of California Sustainable Agriculture and Research Education Program

http://www.sarep.ucdavis.edu/

Reports technical reviews, technical information, and summaries of journal articles and workshop presentations on subjects related to sustainable agriculture.

General agriculture research sites

Purdue University Office of Agriculture Research

http://info.aes.purdue.edu/AgResearch/agreswww.html

Provides a search engine of the agriculture research conducted at Purdue University, some in the area of BBTs.

Biotechnology sites

Biotech-Related WWW Sites and Documents

http://inform.umd.edu:86/EdRes/Topic/AgrEnv/Biotech/.www.html

Provides access to publications and WWW and gopher sites related to biotechnology.

Biotechnology Information Center

http://www.inform.umd.edu:8080/EdRes/Topic/AgrEnv/Biotech

As one of the 10 information centers at the National Agricultural Library of USDA, provides access information services and publications covering agricultural biotechnology, including a bibliography and resources guide, miscellaneous publications, biotechnology education resources, biotechnology newsletters (national and international), biotechnology patents and biotechnology software.

Institute for Biotechnology Information

http://www.bio.com/ibi/ibi1.html

Serves as a database of U.S. biotechnology companies. Includes information on key personnel, R&D, products, budgets, financing history, addresses, and phone and fax numbers. Contains an action database for the significant activities and strategic alliances of biotechnology companies worldwide.

(continued)

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Federal agency sites Address Description

Public Perception of Biotechnology Home Page. Department of Crop and Soil Environmental Sciences and the Center for the Study of Science in Society. Virginia Polytechnic Institute and State University

http://fbox.vt.edu:10021/cals/cses/chagedor/index.html

Offers information on a study of the public perceptions of agricultural and environmental biotechnology, including microbial pesticides.

Advocacy and industry group sites

ANBP http://www.rain.org/~sals/anbp.html

Reports on regulation of natural enemies and offers information on other issues affecting the natural enemy industry through the News Quarterly of the National Bio-Control Industry.

Biotechnology Industry Organization

http://www.bio.com/bc/bio/biohome.html

Provides a list of members of the Biotechnology Industry Organization, a trade association representing biotechnology companies of all sizes (including agricultural biotechnology companies). Includes membership information and access to newsletters.

Pesticide Action Network North America

gopher://gopher.igc.apc.org:70/11/orgs/panna

Offers information on an organization advocating replacement of conventional pesticides. Includes some citations on BBTs.

SOURCE: Office of Technology Assessment, U.S. Congress, 1995.

NOTE: Many of the sources containing information on biologically based pest control are still under construction. The site contents andaddresses were current as of August 1, 1995. This information is subject to change.

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| 69

4Risks and

Regulations

iologically based technologies (BBTs)pose certain risks, some better docu-mented than others. The significance ofthese risks depends on how well the reg-

ulatory structure prevents the high impacts. Sci-entists who study the ecology of natural systemsare most concerned about the effects of intro-duced classical biological control agents on thepopulation dynamics of native species and thefunctioning of ecosystems. Past regulatoryreview by the Animal and Plant Health Inspec-tion Service (APHIS) in the U.S. Department ofAgriculture (USDA) has been erratic and incon-sistent. The U.S. Environmental ProtectionAgency (EPA) has done a better job in its over-sight of microbial pesticides under the FederalInsecticide, Fungicide, and Rodenticide Act(FIFRA), but critics charge that previous thor-oughness and concomitant expense to registrantskept useful products from entering the market.The evaluation of new risks from the release ofgenetically engineered microbial pesticidescould pose a major challenge.

Chapter 4 begins with an examination ofpotential health and environmental effects fromBBTs, summarized in table 4-1. The discussionthen turns to some of the tools that scientists andregulators use to evaluate and rank those risks.

The remainder of the chapter looks at how EPA,USDA, FDA, and state governments decidewhich BBT risks are acceptable.

RISKS FROM BBTSBBTs generally receive favorable ratings fromthe perspective of public health and environmen-tal safety. Many are relatively host specific,affecting primarily the targeted pest. Unlike con-ventional pesticides, most BBTs lack mamma-lian toxicity or pathogenicity. Moreover, thedevelopment of resistance by weed and insectpests appears significantly slower for most BBTsthan for conventional pesticides. Despite thesemultiple advantages, the risks from BBTs occa-sionally may be substantial, and therefore theiruse deserves scrutiny and, in some cases, long-term monitoring.

❚ Human Health EffectsHuman exposures to certain BBTs may occur atmany stages of production and application of theBBT and during use of the end product. Forexample, farm personnel and local residents mayinhale microbial pesticides during aerial spray-ing; kitchen staffs and schoolchildren may workand study in facilities treated with tiny wasps and

B

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nematodes; consumers may unknowingly con-sume microbial pesticides and fragments ofarthropod natural enemies in foods, in addition topieces of the pests themselves. Persons whowork in facilities for rearing natural enemies mayface occupational exposure to the insect preda-tors and parasites.

Few human health risks from BBTs have beendescribed in the scientific literature. Best docu-

mented are allergic reactions, particularly to fun-gal pathogens (411,420). Workers in insectarieshave developed allergic asthma and rhinocon-junctivitis (nasal inflammatory disease) fromcontact with the eggs, scales, and waste of thearthropod pests and their natural enemies. Respi-ratory and dermal protection may help retardsuch effects (205). Another risk is that manufac-tured microbial pesticides could become contam-

CHAPTER 4 FINDINGS

■ The environmental and public health risks from biologically based technologies for pest control(BBTs) are relatively low when compared to those from conventional chemical pesticides. Never-

theless, BBTs are not risk-free. The significance of the risks depends on how well the regulatorysystem screens out the high impacts.

■ The relative absence of documented harmful ecological impacts attributable to BBTs may be mis-leading, however, given the lack of pre- and postrelease monitoring. Some of the most harmful eco-

logical effects, such as declines in native insect populations, have probably gone unnoticed in pastdecades.

■ The risks from certain BBTs cannot be accurately assessed; some scientists argue that they neverwill be. The wide variation in scientific opinion and the high degree of uncertainty concerning BBT

efficacy and ecological impacts heighten the need for public participation in the regulatory pro-cess. One committee that would benefit from more diverse representation is the Animal and Plant

Health Inspection Service’s (APHIS) Technical Advisory Group on the Introduction of BiologicalControl Agents of Weeds.

■ Past regulation of natural enemies by APHIS was inconsistent and incomplete. Proposed regula-tions were recently withdrawn after APHIS received 252 mostly critical public comments. The

agency needs to devise a regulatory framework that ensures environmental safety while encourag-ing the development and use of BBTs.

■ The regulated community gives the U.S. Environmental Protection Agency (EPA) high marks for thecreation of its Biopesticides and Pollution Prevention Division. The division is developing some

much-needed exemptions and expedited registration processes for certain classes or applicationsof microbial pesticides and pheromones. Ecologists warn, however, that EPA should not go too far

in waiving its environmental testing requirements.■ Many genetically engineered microbial pesticides are making their way through the research and

registration pipeline. Scientists are engineering these products to behave more like chemical pesti-cides, characterized by longer environmental persistence, expanded host range, more toxic mode

of action, and faster kill rate. The tracking and evaluation of environmental fate and impacts maypose significant challenges.

■ The Food and Drug Administration (FDA) plays a role that is as yet undefined in the regulation ofbiologically based technologies. The agency is still trying to identify the scope of its regulatory

responsibilities regarding the use of BBTs in grain storage and food preparation areas. FDAinvolvement may increase significantly as application of these products in urban settings grows.

■ Certain BBTs appear susceptible to resistance, but apparently at a rate slower than that for chemi-cal pesticides. Widespread use of transgenic plants containing toxins from Bacillus thuringiensis(Bt), however, may speed the development of pest resistance to Bt and squander its value as amicrobial pesticide.

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TABLE 4-1: Examples of Potential Risks from BBTs

BBT examples Potential environmental impacts Potential human health effects

Conservation of natural enemies

Probably insignificant No known riska

Classical biological control/introduction of new natural enemies

Some adverse impacts on nontarget organisms; destabilization of existing control by predators and parasites; habitat destruction; possible evolutionary changes. Many of these risks are shared by other BBTs

No known risk

Release of sterile fishes for biological control

Adverse effects on nontarget organisms; potential for hybridization with wild forms; possible development of resistance, self-reproducing strains, or selective mating patterns; potential transmission of parasites

No known risk

Augmentative releases of parasites and predators

Some risks similar to those for classical biological control; contamination of field-harvested natural enemies by parasites; depletion of natural enemies in collection sites

Allergic reactions among workers in insectaries

Pheromones Potential adverse impacts on aquatic invertebrates and some fish from lepidopteran varieties,b but warning labels advise against such usage; other types of pheromones may have greater potential toxicity to mammals, fish, and birds; undocumented possibility for disruption of mating behavior of other insects; slight risk of resistance

Low oral or inhalation toxicity, possible dermal and eye irritation, from lepidopteran-active products; higher toxicity among other pheromone groups, but minimal human exposure

Bacterial pathogens(microbial pesticides)

Some adverse impacts on nontarget lepidoptera and their avian predatorsShort-term declines in certain nontarget insects; resistance documented in field populations of pests treated regularly with Bt

Minimal risk to general population; some data suggest possible infection of immunocompromised individuals

Viral pathogens(microbial pesticides)

Minimal effects on nontarget organisms; possibility of resistance in future as field use expands

No known risk

Fungal pathogens(microbial pesticides)

Possible effects on nontarget organisms; early evidence of resistance

Some established human allergens and toxic metabolites

Protozoan pathogens(microbial pesticides)

Possible effects on nontarget species No known risk

Nematodes(microbial pesticides)

Possible effects on nontarget organisms, particularly those in the soil

No known risk

Release of sterile insects Some adverse effects on nontarget organisms; possible development of resistance, self-reproducing strains, or selective mating patterns

No known risk

a “No known risk” indicates that risks have not been documented. In some cases, the absence of documented effects may be due to a lack ofmonitoring or observation.b Lepidoptera is a large order of insects that includes butterflies and moths, some of which are considered pests.

SOURCE: Office of Technology Assessment, U.S. Congress, 1995.

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inated with human pathogens such as Shigellaand Salmonella; each production batch must bescreened for the growth of unwanted organisms(314).

Health concerns arise more often from micro-bial pesticides than from other biologically basedapproaches. Bacteria, fungi, protozoans, andviruses all raise questions about infectivity; bac-teria and fungi trigger toxicity concerns as well(311). Occasional medical case reports describeinfection from certain microbial pesticides,although it is unclear whether the organismshave actually multiplied or caused any harm inpatients’ tissue (125).

Products based on Bacillus thuringiensis (Bt),by far the most widely used microbial pesticides,have been the focus of many animal experimentsand some human studies. Isolated incidents ofeye infection and inflammation of connective tis-sue have been reported. Some varieties of Bt(esp. israelensis, used for blackfly and mosquitocontrol) are more toxic to mammals than others(e.g., kurstaki, primarily used for gypsy mothand other lepidopteran pests) (125).

Although there is minimal evidence of healthrisks to the general population, some researchershave suggested that immunocompromised indi-viduals (e.g., people with AIDS) may exhibitheightened susceptibility to certain insect patho-gens including Bt (125,311,346). Similar con-cerns apply to individuals undergoingimmunosuppressive cancer therapies (see table4-1).

A BBT use that may call for extra attention inthe future is the application of microbial pesti-cides to agricultural products after harvest to pre-vent spoilage. To date, EPA has registered forpostharvest use only microbial products thatwork by preferentially colonizing wounded tis-sue to the exclusion of microorganisms thatcause rot. These microbial pesticides, such asEcogen’s Aspire (a yeast, Candida oleophila)and EcoScience’s Bio-Save (a bacterium,Pseudomonas syringae), although still present inreduced numbers on citrus, apples, pears, andother fruits at time of consumption, are consid-ered by EPA to be as safe as the microorganisms

regularly residing on these foods (182). Anotherapproach controls microorganisms by producingantibiotic substances that are toxic to a broadrange of organisms. These fungal and bacterialagents, if ever applied to fresh fruits and vegeta-bles, would require a detailed evaluation of tox-icity and pathogenicity, especially toimmunosuppressed people (81,426).

Minor impacts on mental well-being mayresult from at least one natural enemy. The Asianlady beetle, Harmonia axyridis, was released byUSDA from 1916 to 1985 primarily in the south-ern United States to control pecan aphids (288).Despite the lady beetle’s beneficial agriculturaleffects, some people have come to regard theinsect as a nuisance: Lady beetles enter homes inlarge swarms, where they interfere with dailyactivities and emit a noxious-smelling secretion.Anecdotal accounts describe families collectingpints of lady beetles in their homes on a dailybasis and finding lady beetles crawling on theceiling, windows, walls, and beds, and in cups,bowls, coffee pots, and so forth. Many state agri-cultural experts urge homeowners not to kill thelady beetles, in light of the insects’ importantrole as natural enemy of aphid pests (288,252).

❚ Environmental Impacts from BBTsMany of the effects of BBT use remain unknown(313). Natural enemy companies generally pointto an exemplary record of safety (128), whereasconservation biologists argue that the dearth ofdocumented impacts does not mean they havenot occurred (220). There have only been occa-sional studies of environmental effects in theUnited States, and most of these efforts havebeen directed toward agricultural crops. The con-sequences for nontarget native insects, in particu-lar, have been largely ignored (151). Some ofthese play important roles as natural enemies.Yet unlike native plants and commercial crops,insects (with the possible exception of butter-flies, honeybees, and silkworms) have no constit-uency to advocate for their conservation(284,117).

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Despite the incomplete and controversialrecord, at least a few documented releases of cer-tain biological control agents have disrupted nat-ural communities and brought about localizeddeclines in native species. Some of the very char-acteristics that make many natural enemies effec-tive in controlling pests (their capacity to harmother organisms, to survive, to reproduce, to dis-perse, and to evolve adaptations to new condi-tions) also make them potentially harmfulinvaders (219). Generalist natural enemies—those less choosy in selecting food sources,hosts, or mates—pose some of the more seriousecological risks. The level of risk depends alsoon such factors as the reversibility of the release,the potential of the agent to spread, the extent towhich impacts may be mitigated, the availabilityof monitoring, and the predictability of impactsacross life cycle and distribution. It is worth not-ing that some of the more significant adverseimpacts that have resulted from biological con-trol releases took place long ago, and manyinvolved generalist predators on small islandecosystems in other countries. In the analysis thatfollows, OTA’s emphasis is on documentedimpacts in the United States. Where there are noU.S. examples, the text also includes somepotential risks based on experience in othercountries, as well as some of the theoretical riskspostulated by ecologists and other scientists.Many of the introductions of agents that aredescribed would not stand up to scrutiny or beallowed today.

Although the potential consequences from theuse of biological control agents and certain otherBBTs are worrisome, it is worth rememberingthat the pests themselves—and the syntheticchemical methods of control—raise health andecological concerns that at least equal and oftenexceed those presented by most BBTs (414).Consideration should also be given to otheravailable options for controlling a particular pestsituation. The following discussion describes thefull range of documented and theoretical risksfrom BBTs and then puts these risks in context.

Impacts on Nontarget OrganismsIntroduced natural enemies, sterile insects, cer-tain microbial pesticides, and pheromones havesometimes affected not only the targeted pestspecies but also nontarget plants or insects.These nontarget organisms are often related tothe pest species. Some serve important ecologi-cal roles; others are listed by the U.S. Fish andWildlife Service as threatened or endangered.Many of the suspected or known impacts haveoccurred in habitats far and ecologically dispar-ate from the original location of release, and attimes long after the introduction or use of theBBT. The release of classical biological controlagents raises the greatest ecological concerns,although the extent of risk is controversial. Ver-tebrate organisms and other generalist speciespose many of the more important risks; some ofthese are addressed in greater detail in OTA’sreport, Harmful Non-Indigenous Species in theUnited States (338).

The best-documented nontarget impactsinvolve the release of vertebrate predators. Forexample, the barn owl (Tyto alba), imported in1958 into Hawaii from California for rodent con-trol, preys also on shearwaters, terns, petrels, andother organisms (313). The small Indian mon-goose (Herpestes auropunctatus), released in theWest Indies, Mauritius, Hawaiian Islands andFiji, failed to control its target—rats in agricul-tural fields—but caused the decline of nativebirds and, in the West Indies, apparently contrib-uted to the extinction of native snake and lizardspecies (313,284). A predatory snail, Euglandinarosea, introduced to many islands throughout theworld for control of the giant African snail,Achatina fulica, may have helped bring about theextinction of several endemic snails (313).

In some instances, fishes introduced for bio-logical control (including the two most widelyused varieties, mosquito fish—Gambusia spp.,and grass carp—Ctenopharyngodon idella) havecaused substantial declines in local populationsof native fishes (313,338). For example, the mos-quito fish, introduced in many regions for mos-quito control, has preyed on, and in somelocations contributed to the decline of at least 35

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other fish species (313). Seemingly innocuouspredatory fishes may become harmful as theyswitch dietary preferences in later life stages.The use of fish-eating fishes to control pest fishspecies raises special concerns because nativefishes are often highly valued resources (191).

Plant-eating (phytophagous) insects intro-duced for biological control of weeds havespread to other locations where they have con-tributed to the decline of related native plant spe-cies. A few such cases are documented, butothers may have gone unnoticed. One example,that of the cactus moth (Cactoblastis cactorum),a native of Argentina, illustrates the need to eval-uate the effects of a candidate biological controlorganism on all potential plant hosts. The moth,which feeds only on cacti of the genus Opuntia,was released with great success as a biologicalcontrol agent in Australia (1925), on several Car-ibbean islands (1957, 1962, and 1970), and inother locations. Together with two scale insects(Dactylopius species), the moth effectively con-trols highly invasive weed species of the cactus,for which chemical pesticides, grazing, burning,and other approaches are economically and envi-ronmentally infeasible (75). The moth has hadserious nontarget impacts on native Opuntia spe-cies on Nevis and Grand Cayman; at the time ofits release, however, the value of these indige-nous plants was not fully appreciated (74).

After dispersing on its own through Haiti, theDominican Republic, Puerto Rico, the Bahamas,and Cuba, the cactus moth eventually entered theUnited States, possibly as a contaminant of horti-cultural stock (220). The moth was discovered inFlorida in about 1989. In the Florida Keys itlargely destroyed the few remaining stands of thesemaphore cactus (Opuntia spinosissima), a can-didate for listing under the Endangered SpeciesAct. This development probably would havegone unnoticed had it not taken place on aclosely monitored Nature Conservancy preserve(313,284). It is likely that the cactus moth willspread north through Florida and west into Texas

and Mexico, where it may attack other Opuntiaspecies, including weeds, food or feed crops, andecologically valuable species (75).

Numerous anecdotal accounts, intenselydebated but often poorly documented, describebiological control agents that have parasitizednontarget insects in Hawaii, Fiji, and NewZealand (313). Most of these releases occurred inprior decades.

A documented example of nontarget effectsfrom a microbial pesticide involves certainstrains of Bt that can harm nontarget Lepi-doptera1 (313,220). Secondary effects on insect-eating bird species are possible: The decline infood may force them to change location or maydepress successful reproduction (283). Someresearchers suggest that the decline in nontargetLepidoptera may be only temporary (411), possi-bly because the Bt does not form free-living pop-ulations (158).

One realm of particular concern involvespotential risks in using plant pathogens for agri-cultural weed control. Farmers usually face acomplex of broadleaf and grassy weeds. Devel-opment of a microbial pesticide containing suffi-cient variety of organisms to control severalweed species would require a dauntingly com-plex set of tests to ensure safety. This situationcontrasts with that of rangeland noxious weedcontrol, in which land managers may target aparticularly troublesome weed species individu-ally (167).

The introduction of natural enemies to controlnative pests, however, raises concerns becausethe full ecological role of the pests may not bewell understood. Certain native plants that arepests in one context may also be an importantsource of forage and may support numerousother native species. Debate about the desirabil-ity of using introduced biological control agentsagainst native species rose to the surface in 1993.Plans by federal researchers to use a wasp para-site and a fungal disease against rangeland grass-hoppers ground to a halt when entomologists

1 Lepidoptera is the insect order that includes butterflies and moths.

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Use of introduced natural enemies against native pests, suchas this weevil (Heilipodus ventralis) on snakeweed (Gutierreziasarothrae), is controversial because of potential impacts onnative ecosystems,

Agricultural Research Service, USDA

pointed out that the control agents might alsoaffect many of the over 280 nontarget nativegrasshoppers (122). Some may play importantroles in native ecosystems, for example by sup-pressing native weeds such as snakeweed. Thecase continues to be highly contentious amongscientists (204,43).

Interference with Existing Control Agents–Competition and Life-Cycle DisruptionSome evidence suggests that biological controlagents have adversely affected native naturalenemy populations by outcompeting them forfood or other resources. Such competition isnotoriously hard to document in the field, partic-ularly among insects, the habitats and behavioralpatterns of which are not well studied (313). Afew such situations have been reported, one con-cerning the European lady beetle (Coccinellaseptempunctata), which has been released widelyin the United States. The introduced lady beetleappears to be displacing other predatory insectssuch as the nine-spotted lady beetle (C. novem-notata), thereby potentially disrupting the controlof pests by native insects (313). In fact, the Euro-pean species is now the dominant lady beetle byfar in many of the agricultural systems it has col-onized (170).

Biological control agents can affect nontargetorganisms also by interfering with their lifecycles, ultimately resulting in the upsurge of pestpopulations. Reports from Fiji describe the life-cycle disruption of the coconut leaf-mining bee-tle (Promecotheca reichei) by an introduced mite(Pediculoides ventricosus), reducing the popula-tion of native parasites and thus enabling the bee-tle population to skyrocket (313).

Habitat DestructionDamage to the habitats of nontarget species is animportant yet underreported risk from the intro-duction of fishes for aquatic weed control. Thesefishes dramatically reduce local plant cover,potentially causing significant disruption to bothplant and animal communities (313). In the caseof grass carp, however, the negative impactshave been reduced somewhat by only using thefish in enclosed water bodies and by releasingsterile triploid fishes (191). The U.S. Fish andWildlife Service operates a certification facilityto ensure that grass carp for biological controlare unable to produce viable offspring, and moststates require permits and verification of trip-loidy for grass carp imports (191). The approachis impractical for many fish species, however,and generally not all fish in a treated lot becomesterile (313). Although individual fish that arereleased harm nontarget vegetation, as do theirfertile counterparts, the sterilized fish usuallywill not form reproductive populations that canspread.

Reproductive EffectsA little-documented potential risk from phero-mones is the disruption of mating patterns. Thereis some evidence that the pheromone of barkbeetles that stimulates them to flock togethermay influence the behavior of other beetles. Sexpheromones of Lepidoptera may possibly affectthe behavior of certain parasites (313).

Another reproductive concern relates to theuse of immunocontraceptive control for verte-brate pests, although these approaches have notyet been used in the United States. Australia

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plans to use genetically engineered viruses tocontrol foxes and rabbits by inducing thefemales’ immune system to attack male sperm.The control plan will require simultaneousdepression of both fox and rabbit populations:Controlling only the foxes would enable the rab-bit population to explode; restricting only therabbits would induce the foxes to switch to otherprey, most likely endangered marsupials. Austra-lian scientists are examining potential risksincluding the capacity of live infectious virusesto multiply, to attack other species includinghouse pets, and to spread abroad.

The rabbit control involves a redesigned myx-oma virus, which is specific to rabbits and hares.Lacking a virus specific to foxes, the Australiansrisk inadvertently sterilizing dingoes (wild dogs)and domestic dogs. Similar concerns have beenraised by researchers at APHIS’s Denver Wild-life Research Center, who are developing immu-nocontraceptive therapies with which to sterilizecoyotes and deer in the United States (225).

❚ Other Potential Risks

Evolutionary Change among BBTsEvaluating genetic change among populations ofbiological control agents after their introductionis difficult and has rarely been attempted (171).Yet some ecologists argue that the conditions ofsuch releases facilitate the rapid evolution ofchanges in a natural enemy’s host range or otherimportant characteristics. Evolved resistance toconventional pesticides occurs with some fre-quency among arthropods and has been demon-strated experimentally in certain natural enemies(see chapter 2). Introduced species might alsoevolve an expanded tolerance of physical factors,thereby increasing the range of habitats they mayoccupy and thus their impacts (313).

Some scientists speculate that biological con-trol relationships could become less and lesseffective over time as the pest and its naturalenemy evolve in response to one another (313),although data are lacking on the likelihood andon the rate at which this might occur. A furtherpossibility is that introduced species might

hybridize with native ones to the point that thenative species no longer exist in their originalform. Little research has addressed this phenom-enon. The one documented case involved theintroduction of mosquito fishes (Gambusia affi-nis and G. holbrooki) that hybridized withanother related species (Gambusia heterochir)and now threaten the integrity of the latter’s genepool (313).

Inadvertent Introduction of Parasites of Natural EnemiesAPHIS’s screening of incoming biological con-trol agents generally prevents accidental impor-tations of hyperparasites (i.e., parasites ofparasites) (236). A unique example of hyperpara-sitism among field-collected biological controlorganisms in the United States concerns the ladybeetle (Hippodamia convergens). A parasiticwasp may contaminate up to 10 percent of theselady beetles. In the spring of 1994, APHISdecided to prohibit interstate shipment of field-collected lady beetles that had not been held inquarantine and cleared of parasites. Followingstrong public protests arguing that the collectionand dispersal of California lady beetles has beena cottage industry for over 75 years and is thusunlikely to cause further adverse effects, APHISoverturned the decision. The agency continues tourge that field-collected lady beetles be held toidentify and remove parasitized individuals (60).

Resistance to BBTsPest resistance to conventional insecticides hascontributed to the growing interest in biologi-cally based approaches. Initial findings suggestthat pests may develop resistance to certainBBTs, particularly bacteria and viruses (9,411),and possibly fungi (420,281) and pheromones(40) as well. The likelihood of resistance or rateat which it might develop is unclear however.Compared with conventional pesticides, mostBBTs appear less prone to stimulate resistance.Many biological approaches benefit from physi-ological modes of action (such as interferencewith photosynthesis, respiration, transpiration,

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translocation, and seed production) that make itmore difficult for pests to develop resistance toBBTs than to certain conventional pesticides thatlack these properties (420).

If pests become resistant to BBTs, makingthese approaches no longer effective, agriculturewill lose an important set of low-risk pest controltools. Indirect health and environmental riskscould result if growers were forced to switchback to conventional pesticides, because BBTsoffer significant advantages from an environ-mental and public health standpoint (274).

The bacterial insecticide Bt faces the greatestthreat. Future large-scale use of crop plantsgenetically engineered to contain the Bt toxincould speed the development of resistance andput at risk its effectiveness as a microbial pesti-cide (112). Unlike Bt sprays, which are appliedonly intermittently, plants bred to contain Bttoxin in their tissues continuously expose pests tothe toxin over the entire growing season. Thisincreased exposure to Bt heightens the selectivepressure on pests and may hasten the develop-ment of resistance (422,221,146,214). Some sci-entists believe that resistant pest populations willappear soon after the transgenic Bt crops areplanted.

Thus far, evidence of Bt resistance in theUnited States has been seen only in field popula-tions of the diamondback moth (Plutella xylos-tella). Resistance in the moth has been observedin the Pacific Rim, Florida, and New York(411,326). The Colorado potato beetle (Leptino-tarsa decemlineata) on Long Island, New York,which was one of the first agricultural pests todevelop insecticide resistance (to arsenicals inthe 1940s and to DDT in 1952), now shows thepotential for resistance to Bt tenebrionis. The sil-verleaf (sweet potato) whitefly (Bemesia argenti-folii ), another major pest that is notoriouslydifficult to control because of its expandingresistance toward organophosphate, carbamate,and pyrethroid insecticides, has developed resis-tance to Bt kurstaki in Taiwan, the Philippines,and Malaysia (112).

There is no published evidence of an insectdeveloping resistance to a virus in the field.

Microbial pesticides based on viruses have notyet been used extensively in the United States.Lab results indicate, however, that future large-scale use might result in resistance (411).

The potential that pests will develop resis-tance to other BBTs is only speculative at thistime. Continuous exposure of susceptible insectpests to nematode products, for example, mightencourage selection for resistance (411). Theo-retically, pest populations might even evolveresistance to the sterile male technique by devel-oping self-reproducing strains or the ability torecognize and mate only with fertile males (313).

Depletion of BBT Agents in Natural AreasThe mass collection of natural enemies impactsregional populations. Unlike most augmenta-tively released natural enemies, which are raisedin insectaries, the lady beetle (Hippodamia con-vergens) and several natural enemies of range-land weeds are collected from field sites. Thelady beetles, for example, are harvested fromlocations in the California foothills to which thebeetles migrate. Lady beetles dominate the bio-logical control market for garden use because oftheir familiarity to the public, promising anec-dotal stories, aesthetic appeal, and long history ofcommercial sale. Despite some doubts as to theireffectiveness (see box 3-1 in chapter 3), the col-lection and sale of lady beetles continues toincrease, with demand often exceeding supply.Supplies are finite, however, and there areincreasing concerns about environmental costsassociated with the commercial collection of theinsect (60). In addition, the collection under-mines natural control, which is free to the farmer(416), and interferes with publicly supported bio-logical control programs.

Genetically Engineered BBT OrganismsThe environmental repercussions of geneticallyenhanced microbial pesticides deserve specialscrutiny. Scientists are using genetic engineeringtechniques to expand the target range (194),incorporate more toxic modes of action, increasekill rates, and extend environmental persis-

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tence—in essence, to make microbial pesticidesmimic their more heavily regulated chemicalcounterparts. Implications for nontarget speciesmay grow in future years as these products movethrough EPA registration. University of Floridaentomologist J.H. Frank (1995) raises concernswith respect to genetically engineered Bt prod-ucts (108):

Research is attempting to increase the rangeof targets that Bt will kill, to increase commer-cial profitability.... Where will it stop—howbroad would commerce like the target range tobe? Why should these commercial interestsbother to look out for the welfare of nontargetorganisms? Even more, why should they lookout for the welfare of beneficial organisms thatalready exert partial control of some pests andcomplete control of others? It is not in theirinterests to do so, because they will be able tosell more product in the absence of these benefi-cial organisms....

The interests of commercial profitability andthe protection of nontarget species may collideover the issue of target range. From an environ-mental perspective, a key advantage of manyBBTs is their relatively narrow range of impacts.Yet products that kill or impair a wider range ofspecies cater to a larger pest control market andhence generate higher profits. Producers ofgenetically engineered BBTs are developingmicrobial products with extended target range,although whether their breadth will ever rivalthat of conventional pesticides remains to beseen.

Some of the environmental effects from genet-ically engineered BBTs remain unclear. Depend-ing on the properties of the toxins or hormonesinserted into the microbe to achieve pesticidalactivity, for example, symptomless infections bygenetically modified viral insecticides in nontar-get organisms could go undetected and later pro-vide a reservoir of infection of other organisms(429).

❚ Putting the Risks in ContextAlmost every scientist contacted by OTA aboutBBT risks prefaced his or her comments byemphasizing that the occupational and environ-mental risks from conventional pesticides dwarfthose from biologically based approaches. Forexample, chemical insecticides, herbicides, andfertilizers have caused documented adverseimpacts on more than 90 species listed under theEndangered Species Act (89), as well as serioushealth and ecosystem effects. Although beyondthe scope of this report, the risks from these syn-thetic pest control methods help put into perspec-tive the relative safety of most BBT options.

The relative absence of effective low-risk pestcontrol solutions—perhaps intercropping, croprotation, field sanitation,2 and row covers wouldfall in such a category—suggests that difficultchoices must be made among suboptimaloptions, each of which implies an array of haz-ards for different organisms and population sec-tors. The risks differ both qualitatively andquantitatively: Chemical pesticides raise signifi-cant consumer and occupational health issues, inaddition to environmental effects, whereas BBTsaffect primarily native species, and native biodi-versity is a relatively new category of concern inthe United States.

Important risks derive also from failure tocontrol the pests. These organisms, many ofthem invaders from foreign lands, can damageeconomic resources as well as native ecosystems.Our nation’s food supply depends on efficient,low-cost agricultural technologies, and our envi-ronmental and aesthetic needs depend on thepreservation of our national treasures such asparks and forests.

Most BBTs have a favorable health and envi-ronmental profile, and some provide solutions topernicious health risks (box 4-1). A well-designed regulatory system could screen out thegreater risks from BBTs while facilitating adop-tion of the vast majority of these technologies.The development of proper recordkeeping and

2 Field sanitation involves the removal of crop residues that harbor pest stages.

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monitoring systems could advance our base ofknowledge, improve the development of newBBTs, and eventually allow for a tighter match

between risks and regulatory testing require-ments.

BOX 4-1: Controlling Public Health Scourges with BBTs

Biologically based approaches can sometimes control the disease vectors or intermediate hosts ofmalaria, schistosomiasis, and other afflictions of humans and livestock. Fishes, turtles, and fungi, for

example, have all been used to control mosquitoes that transmit malaria and dengue fever in the tropicsand veterinary diseases, such as heartworm and equine encephalitis, in the United States. The use of

BBTs for public health purposes has certain advantages but also raises potential problems.

Over 200 fishes from around the world are known to eat mosquito larvae. In addition, fish that eataquatic vegetation may modify their habitats, making them less suitable for mosquitoes. A big advantage

of using fish for mosquito control is that they generally require little investment or infrastructure to producean acceptable level of long-term control. In addition, the potential to evolve resistance to fish predators is

much less than that to insecticides.

Although sometimes quite effective, however, fish do not completely eliminate mosquito populations;

generally they do not provide the level or the rapidity of control achievable with insecticides. Their use isrestricted to suitable bodies of water, leaving out many important mosquito habitats. Moreover, the non-

target impacts can be severe. The fish most commonly used for mosquito control in the United States, forexample, is the mosquito fish, Gambusia affinis, from the southeastern United States. This fish often out-

competes other native fishes. Mosquito fish develop dense populations and may reduce the foodsources or eat the eggs and young of native species.

Fungal species of the genus Coelomyces and Lagenidium are lethal to mosquitoes. The spores pene-

trate the insect and can cause mortality within a few days. Areas can be inoculated with fungal pathogensby transporting infected insects or sporangia to the target location. A significant advantage of fungal

pathogens over the use of insecticides or Bt is that mosquitoes are less likely to evolve resistance tofungi. Moreover, since the fungi are already widely distributed worldwide, there may be less concern

about unpredictable damage to nontarget species.

Fishes and fungi are not the only possible control agents for mosquitoes. Bats and some birds, suchas swallows, consume an extraordinary number of mosquitoes, and juvenile turtles have reportedly pro-

vided successful control of mosquitoes in cisterns for drinking water in Honduras.

Schistosomiasis is another cause of considerable morbidity and mortality in the developing world.

Certain predatory fishes can effectively control juvenile snails such as Biomphalaria glabrata, an interme-diate host for the parasitic worm that causes the disease in the tropics. In addition, a competitor species

of snail, Marisa cornuarietis, is used as a control agent in Puerto Rico and is considered to have contrib-uted substantially to the sustained reduction of schistosomiasis on that island; adverse ecological

impacts have not been documented. In Florida and other regions, however, the snail feeds indiscrimi-

nately on many native plant species.

SOURCES: A. Kuris, Department of Biological Sciences and Marine Science Institute, University of California, Santa Barbara, CA,“A Review of Biologically Based Technologies For Pest Control in Aquatic Habitats,” unpublished contractor report prepared forthe Office of Technology Assessment, U.S. Congress, Washington, DC, October, 1994; D. Simberloff, Department of BiologicalSciences, Florida State University, Tallahassee, FL, letter to the Office of Technology Assessment, U.S. Congress, Washington,DC, July 16, 1995.

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In the real world, moreover, many of the pos-sible risks from BBTs pale in comparison withthe benefits of use. For example, in the case ofcoddling moth control, although scientists havepostulated theoretical risks with regard to futureimpacts of pheromones on the mating behaviorof introduced natural enemies, in practice so farsex pheromones have proved to be highly effec-tive in concert with augmentative releases of Tri-chogramma wasps. Studies on cotton bollwormand European corn borer suggest that the pres-ence of certain pheromones actually enhancesthe searching behavior of the wasps (236).

Risks that deserve particular scrutiny in thenear future include the growing resistance to Btand the potential to rapidly reduce its effective-ness through large-scale use of crop plants con-taining Bt genes; the untested ecologicalrepercussions from the use of genetically engi-neered microbial pesticides; and, more generally,the effects of BBTs on insect populations, organ-isms that often play valuable ecological roles andserve as natural enemies of many household andagricultural pests.

❚ Minimizing the RisksRegulatory agencies use several tools to sort outwhich BBTs bear more significant risks and toexpedite registration of the safer technologies.Many of these tools have not yet been fullydeveloped. A brief explanation of some of theseapproaches follows.

Establishing Priorities for Risk Evaluation and TestingRisk depends on the level of hazard as well as theextent of the exposure. Evaluation of BBT risksshould consider each of the possible adverseimpacts plus the risk from the uncontrolled targetpest and from other pest control approaches.Some scientists suggest that a ranking of BBTsalong risk categories could help agencies set pri-orities and fast-track the permit applications ofthe most promising and least risky BBT candi-dates. By using more of a tiered testing system—in which more rigorous testing is only required

when a potential risk is detected—agencies couldstreamline the data requirements for safer BBTproducts.

Developing a hierarchy among risks is contro-versial, often difficult, and sometimes impossi-ble. It is not easy to generalize risk categories.The rankings may reflect scientific assumptionsabout the breadth of the host range, as well asbroader assumptions about the value to beassigned particular classes of nontarget organ-isms (219). They could also include patterns ofuse and likely levels of human exposure.

Most scientists would place terrestrial verte-brates at the top of the risk hierarchy. Introduc-tions of organisms such as the mongoose, mynabird, and giant toad have had severe and wide-spread adverse impacts due to their nonspecificfeeding and their numerical abundance (219).

Many researchers would also designate ashigh risk those organisms that feed on a widerange of plants and animals (284). Generalistfeeders such as the sevenspotted lady beetle(Coccinella septempunctata), which APHISdecided to mass-rear as a biological control agentin the late 1980s, have displaced native species inmany environments (169). Even a nontargetorganism that is rare or endangered—and there-fore would not sustain a predator population—may still be vulnerable if related species in thevicinity that are more abundant attract the gener-alist agents (220).

Among control organisms used against arthro-pod pests, predators tend to be less host specificand less successful in biological control pro-grams than parasites, suggesting that parasitesdeserve a lower place in the hierarchy of risks(219). Advantages of parasites include theirgreater specificity, searching ability, and abilityto persist along with the pest at low populationlevels. Nonetheless, there may be reasons to usepredators instead: Their lower specificity andtheir capacity to switch from one type of prey toanother may produce more effective control offluctuating pest populations (219). Also on thelow end of the risk spectrum could be suchapproaches as the conservation of natural ene-mies or the use of pheromones in traps.

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A major difficulty with attempting to order thelevels of risk, of course, is that there will alwaysbe exceptions. Organisms within categories des-ignated as high risk may prove relatively innocu-ous, while those that fulfill the criteria as low-risk BBTs may cause unexpected harm. A regu-latory system that incorporates reliance on riskcategories, therefore, must also include flexibil-ity and substantial safeguards to ensure the rec-ognition of such exceptions.

An advantage of a risk hierarchy is that itfacilitates matching the required pre-use evalua-tions to the likely level of risk posed by a BBT.Evaluation schemes that take into account thevariable levels of scrutiny required by differentpotential risks are called tiered testing. Thesesystems preclude unnecessary testing and wastedresources. APHIS and EPA use tiered testing tovarying degrees. The first tier provides maxi-mum opportunity for the identification of anyadverse effects. BBTs that pass the first tier arenot subject to further testing. Second and thirdtier testing are used to reveal possible mitigatingfactors (21 9).

Testing for Host SpecificityHost specificity measures the degree to which abiological control agent is restricted to its target.It provides information on the range of organ-isms a biological control agent will affectthrough feeding, reproduction, or other interac-tions. Scientists use information on host specific-ity to try to identify the organisms likely to beattacked by candidate control agents in therelease environment. Testing of host specificitybegan for biological control agents targetingweeds in the 1950s. Initially, the potential agentwas tested only on the agricultural crops growingin the region into which the control organismwas considered for introduction (21 9).

More predictive frameworks have sincereplaced the crop-testing method, often placinggreater emphasis on nontarget threatened andendangered species and other plants of ecologi-cal value. Many biological control practitionersadvocate use of the centrifugal/phylogenetic

Natural enemies imported for research on the biological controlof weeds are held in quarantine prior to release.

Agricultural Research Service, USDA

approach, which involves testing plants ofincreasingly distant relationship to the targetuntil the host range is circumscribed. The centrif-ugal approach is not without its problems, how-ever. For one, it assumes that related plants aremore likely to be attacked, whereas, in reality,sometimes widely unrelated plants are attacked(220). This may be more a problem amongpathogens than among insects (159). In addition,the centrifugal approach may overlook someimportant variations in resistance and suscepti-bility of individual hosts (328).

The relatedness procedure, the newestapproach to host specificity, is a subtractive pro-cedure that involves selecting plants to be testedon the basis of their evolutionary relationship tothe target organism, as well as their distribution,climatic preferences, seasonal occurrence,regional weather patterns, life cycles, and otherinformation available in the scientific literature(73). The approach is weighted to favor thosepotential hosts most closely related to the targetorganism, but it tests representatives from allother levels of relationship as well. The methodhas been applied successful y in Australia for thehost-specificity testing of Uromysces heliotropic,a fungal agent for the biological control of theweed, common heliotrope, Heliotropism euro-paeum (139,140,73).

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The relatedness procedure or other host-speci-ficity approaches, if better developed in thefuture, may make possible the use of shorter,more predictive and reliable testing lists (73). Todate, however, the science of host specificity hasa long way to go, particularly given the complex-ity of ecological interactions and the difficulty ofmeasuring them (360).

APHIS and EPA rely on these various testingprocedures to varying degrees. APHIS evaluatesthe data on the basis of whatever approach theresearcher uses. If a researcher asks for guidanceon host range testing, the agency sends two sam-ple papers, one from 1974 based on the centrifu-gal procedure and one from 1992 based on therelatedness procedure (360). In practice, how-ever, the choice of nontarget test organismsdepends more often on what the researchers hap-pen to have available or readily accessible andknow how to test (159,73). EPA’s testing proto-cols emphasize the major agricultural crops.

Another problem is that researchers develop-ing test lists for BBT registration applicationsoften have little background in relevant biologi-cal disciplines. Entomologists petitioning tointroduce an arthropod species that attacksweeds, for example, commonly lack the botani-cal training needed to identify likely host plantsbased on evolutionary relationships, life cycles,and other aspects of plant ecology (159).

Because of their potential to attack agricul-tural crops, pathogens of plants and plant-eating(phytophagous) arthropods have traditionallyevoked the most thorough host-specificity stud-ies. Host-specificity assessment for predators,parasites, and pathogens of insect pests, by con-trast, remains in an early stage of development.This situation reflects the lower degree of social,economic, and environmental concern for arthro-pods than for plants as nontarget organisms.There are far fewer “domestic” arthropods (suchas honeybees and silkworms) than there are agri-cultural crops, and plants are far more likely tobe listed as threatened or endangered species,thus deserving special protection. Many scien-tists argue that the biological control agents used

for control of arthropods deserve more carefulattention than they receive today.

A single species that feeds on several organ-isms is often made up of numerous more special-ized individuals. Such diverse populations mayharbor enough genetic variation to evolve andeventually change hosts. Thus testing shouldsample as much genetic and geographic variationin the biological control agent as possible, tomaximize chances of detecting the variationamong individuals upon which natural selectionmight act (219).

Host RangeHost range refers to the number of different spe-cies that a given agent will attack. Although con-ceptually similar to host specificity, host rangefocuses on the biological control agent ratherthan the target. Often the terms are used inter-changeably; they refer to overlapping subsets ofrisk (73).

Examination of a biological control agent inits site of origin provides a basis for predictingeffects in the release area (256); so does informa-tion on the agent’s biology, taxonomy, and ecol-ogy (415). To help approximate the range oforganisms a biological control agent or microbialpesticide will affect in its proposed area ofrelease, however, researchers also use laboratoryand field tests. Lab tests aid in approximating thephysiological host range of the control organ-ism—the maximum extent to which an agentcould impact potential hosts. Artificial testingconditions—such as use of starved biologicalcontrol organisms and lack of dietary choice—may inflate the range results for many arthropodsand pathogens (219). For example, if a candidatebiological control agent does not feed on a testorganism in laboratory conditions, it is nearlycertain that it will not feed on the organism infield conditions. If the biological control agentdoes feed on the test organism in laboratory con-ditions, however, it does not necessarily followthat the same behavior will take place in the field(360).

The actual, or “ecological,” host range isalways less than the physiological host range

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(74). Field tests give a more accurate picture ofthe extent to which control organisms can beexpected to attack nontarget species uponrelease. The accuracy of extrapolation from thephysiological host range (revealed in the lab) tothe ecological host range (revealed in the field)needs improvement. Further development andtesting of host specificity protocols may betterestablish what fraction of the potential host rangeis likely to be expressed in the field (219,73).

Host-specificity and host-range testing are noguarantees of environmental safety. The harmfuleffects of the biological control organism caninclude not only eating, parasitizing, or infectinga nontarget organism, but also indirect effectsfrom interfering with shared natural enemies orshared hosts (219). There is also the risk of inter-species mating, especially with threatened orendangered species.

The relative specificity of BBTs requires thatthey be weighed on a case-by-case basis, eachsituation reflecting a unique set of potential inter-actions among the control organism, targetorganism, and potential nontarget organisms. Nostandard set of indicator species or single repre-sentative sample of nontarget species (e.g.,rodent or other model organisms) or nontargetecosystems will apply to all proposed agents.Moreover, when potential harm to ecosystems isweighed, there may be no easily defined end-points to the analysis, a factor that makes devel-opment of protocols problematic (219).

Evaluating the Risks and Benefits of BBTs and AlternativesRisk-benefit assessment of BBTs is exceedinglydifficult, given the lack of accurate quantitativedata on either risks or benefits. To date, much ofthe available information is unsubstantiated andanecdotal.

Moreover, risk implications may differ withthe purpose of the BBT release. Natural areamanagers usually focus on protecting a largenumber of valued native species, and thus prefernarrowly targeted pest control methods. By con-trast, an individual farmer, rancher, forester, orother producer focuses on the productivity of just

a few species. The use of BBTs with lower hostspecificity may better meet these broad-spectrumneeds, but at the same time may involve greaterecological risks (284).

Many difficulties complicate the task of quan-tifying the relative risks posed by a BBT releaseand those posed by taking no action against thepest or using other control methods. Benefits andcosts may be unevenly distributed socially, geo-graphically, or across generations, and excessiveuncertainty or questionable valuation techniquesmay undercut the analysis (219). A qualitative,multi-factoral comparison of BBTs with othercontrol methods, however, might serve to eluci-date some important differences in nontargeteffects, impacts on groundwater, residues oncrops, and occupational exposures, as well asshort- and long-term effectiveness and resis-tance.

ADDRESSING THE RISKSThis section examines the regulatory structurefor most BBTs. The agencies that regulate BBTshave a difficult dual mission: facilitating thedevelopment and registration of biologicallybased technologies while minimizing the risk ofharmful environmental and public healthimpacts. The incongruous nature of these direc-tives suggests that neither will be satisfied com-pletely. The challenge is to incorporate areasonable degree of ecological scrutiny into amore streamlined and efficient regulatory pro-cess.

Although there is no federal statute thatdirectly deals with biologically basedapproaches, several federal agencies regulateBBTs. EPA oversees the commercial sale anduse of microbial pesticides and pheromones.USDA’s APHIS regulates the introduction anddissemination of biological control agentsincluding arthropods, mites, nematodes, slugs,snails, and other macroorganisms. FDA monitorsthe use of BBTs that could become componentsof stored or prepared food, such as microbialproducts and fragments of insect natural enemiesin stored grain. The U.S. Department of Inte-

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rior’s Fish and Wildlife Service (FWS) evaluatespotential impacts of certain biological controlorganisms on threatened and endangered species.Some states regulate BBTs as well (box 4-2).

This section does not cover in detail regula-tions for the use of vertebrate animals and fishes

as biological control agents. Such agents histori-cally have posed some of the greatest risks, yetthey are subject to very little scrutiny by federalagencies. Instead, most authority resides with thestates (box 4-3).

BOX 4-2: Regulation of BBTs by Hawaii and Other States

Importation or interstate movement of biological control agents requires filing of APHIS’s Application

and Permit to Move Live Plant Pests and Noxious Weeds (PPQ form 526). Before APHIS issues a permit,state regulatory officials have the opportunity to review the APHIS recommendation. In addition, state offi-

cials may indicate special conditions of entry, containment, and release. In general, however, states lackresources to enforce additional requirements.

Seven states have statutes or regulations governing the entry, distribution or release of biological con-

trol organisms into or within their territories: California, Florida, Hawaii, Indiana, Nebraska, North Carolina,and Wisconsin. All of these states will accept PPQ form 526 in lieu of their own permit applications. Many

of the specific state provisions are similar to those required by PPQ; California has explicit lists of biologi-cal control agents not subject to state permit requirements.

At least one state, Hawaii, imposes requirements more restrictive than federal APHIS regulations.Hawaii’s special efforts to keep out certain species stem from that state’s history of ecologically harmful

introductions to its unique and vulnerable island ecosystems. Hawaii maintains lists of prohibited,restricted, and conditionally approved organisms.a Biological control agents not yet listed may be eval-uated for host specificity and other characteristics in the state quarantine facility. Advisory subcom-mittees (on entomology, invertebrate and aquatic biota, land vertebrates, microorganisms, or plants)review applications for introduction of nondomestic animals and microorganisms for biological con-trol and other purposes. The Advisory Committee on Plants and Animals holds bimonthly publicmeetings to decide whether to permit particular agents for biological control or other purposes.

Although Hawaii has instituted elaborate screening procedures, the state is unable to fully enforce itslaws. The Alien Species Prevention and Enforcement Actb provides that USDA will inspect mail enteringHawaii from the mainland United States to prevent the entry of plant materials subject to U.S. quaran-tine laws. APHIS carries out inspections of incoming domestic mail for two hours each day; duringthe rest of the day, however, the mail just enters the state uninspected. Under the Fourth Amendmentto the Constitution, APHIS can open first class mail only with a search warrant; to get one requiresprobable cause. If the inspectors feel or hear (by shaking the parcel) something that seems like plantmaterial, they can use specially trained dogs to sniff it out. If the dogs react to something, that consti-tutes probable cause to obtain a search warrant.

The impetus behind the act was Hawaii’s desire to keep out lizards, snakes, and other organisms fromthe mainland United States that could disrupt Hawaii’s island ecosystem. Yet the act does not actually

apply to these organisms, but only to those listed on U.S. quarantines for interstate commerce. The non-indigenous species of concern to Hawaii damage forests and other natural ecosystems, while U.S. quar-

antine lists focus on risks to agricultural crops. As a result, virtually none of the species of concern toHawaii are included under the Alien Species legislation. APHIS lacks the legal authority to prevent the

entry of these organisms.

(continued)

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Hawaii’s inability to enforce its inspection and quarantine laws illustrates a problem that is universalamong the states: Although the laws are on the books, biological control agents may be shipped acrossthe border illegally. Hawaii’s situation underscores also the difficulties that any state might face in trying toenforce laws more restrictive than federal requirements for the importation and release of biological con-trol agents.

a Chapter 4-71, Hawaii Administrative Rules.b Public Law 102-393 (1992).

SOURCES: J. Levy, Operations Officer, Operational Support, Plant Protection and Quarantine, Animal and Plant Health InspectionService, U.S. Department of Agriculture, Riverdale, MD, personal communication, April 5, 1995; W.W. Metterhouse, Cream Ridge,NJ, “The States’ Roles in Biologically Based Technologies For Pest Control,” unpublished contractor report prepared for theOffice of Technology Assessment, U.S. Congress, Washington, DC, November 1994; “Plant and Non-Domestic Animal Quaran-tine” Title 4, Subtitle 6, Chapter 71 (Non-Domestic Animal and Microorganism Import Rules), Hawaii Administrative Rules, 1995;G. Takahashi, Maritime Supervisor, Plant Quarantine, Department of Agriculture, Hawaii, letter to the Office of Technology Assess-ment, U.S. Congress, Washington, DC, May, 26, 1995; 39 USCA Section 3015.

BOX 4-3: Oversight of Vertebrates as Biological Control Agents

A number of the most harmful past introductions for biological control have involved vertebrate ani-mals. The small Indian mongoose (Herpestes auropunctatus), for example, is renowned for devastatingground-nesting bird populations, chickens, and lizard predators of insects when it was introduced to theWest Indies, Puerto Rico, and Hawaii during the late 1800s. Its importation into the continental UnitedStates has been banned. Other vertebrate animals introduced for biological control in the past, includinggiant toads, ducks, geese, mynah birds, and water buffaloes, have likewise inflicted harm on native spe-cies, and many of these examples would probably not be repeated today.

Several species of fishes continue to be released regularly for biological control, with serious ecologi-cal impacts. The grass carp and common carp (Ctenopharyngodon idella and Cyprinus carpio) that havebeen introduced throughout the United States for weed control also destroy habitats for young fish andincrease water turbidity. Introduction of mosquito fish (Gambusia affinis) not only results in the suppres-sion of mosquitoes, but also has been associated with a decline in populations of certain native fishes.

The standards and mechanisms for regulation of vertebrate introductions differ markedly from thosefor arthropods and pathogens covered in most of this chapter. Under current law, the states retain almostunlimited power to make decisions about which vertebrate animals to import or release. Federal incur-sions in this area have been few and controversial. The state fish and game departments vary greatly inthe rigor and comprehensiveness with which they regulate introductions of vertebrates.

A 1993 review of state laws and regulations revealed that although every state except Mississippi haslaws governing fish releases, at least 15 states lack any legal standards for evaluating species prior torelease. No state ties its releases to any scientifically based protocols, such as those produced by theAmerican Fisheries Society and other organizations, in part because of the costs involved. A number ofstates, however, do specifically prohibit releases of grass carp, and many other states allow only releasesof grass carp that have been sterilized to prevent their reproduction and spread. These provisions, ofcourse, do not address the risks of the more than a half-dozen other fish species used for aquatic weedcontrol in the United States.

SOURCES: Office of Technology Assessment, U.S. Congress, 1993; J.R. Coulson and R.S. Soper, “Protocols For the Introductionof Biological Control Agents in the U.S.,” Plant Protection and Quarantine, Volume III, (R.P. Kahn, CRC Press, 1989); D. Simberloffand P. Stiling, Department of Biological Sciences, Florida State University, Tallahassee, FL and University of Southern Florida,Tampa, FL, “Biological Pest Control: Potential Hazards,” unpublished contractor report prepared for the Office of TechnologyAssessment, U.S. Congress, Washington, DC, January 1994.

BOX 4-2: Regulation of BBTs by Hawaii and Other States (Cont’d.)

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❚ Animal and Plant Health Inspection ServicePast oversight of introduction of biological con-trol agents by APHIS was unbalanced, incom-plete, poorly documented, and difficult tounderstand for those seeking permits. Theagency has taken some promising initiatives inrecent years, however; these include increasedattention to the environmental impacts of biolog-ical control agents of arthropod pests; an effort toconsolidate the agency’s multiple sources ofjurisdiction; an attempt to centralize and makesense of the meager, vague, mixed-up records ofpast permitting decisions; the implementation ofgenus-level permitting; and an ongoing effort toadapt and clarify the permit system for environ-mental releases to better meet the requirementsof the National Environmental Policy Act.APHIS staff deserve praise for these initiatives.Less successful, however, have been recentattempts to impose regulatory structure wherenone existed before (box 4-4). APHIS’s pro-posed rule on the introduction of nonindigenousorganisms attempted to screen out harmfulorganisms, but many people felt that the screenimposed was so fine-meshed as to be virtuallyimpenetrable, thwarting the continued produc-tion, distribution, use, or research of biologicalcontrol organisms.

Outside observers have commented thatAPHIS should not both regulate and promotebiological control. It is difficult to know the sig-nificance of this dual role, although clearly itmay lead to internal tensions and inconsistentmissions within the agency (see chapter 5). Thedebate over the proposed rulemaking revealedsome of these different perspectives. In 1992 theformer APHIS Administrator asked the agency’sNational Biological Control Institute to examinethe agency’s authority in biological control, meetwith interested parties, and propose guidelinesfor the importation, interstate movement, andrelease of biological control agents. The National

Biological Control Institute developed protocolsbased on its two years of discussions with partic-ipants in the biological control community.Although, according to the APHIS Administra-tor’s Office, this preliminary work was acknowl-edged in the rulemaking (216), it appears thatfew of the recommendations were actually incor-porated into the final proposal. Following with-drawal of the proposed rule, APHIS formed anew task force that includes the National Biolog-ical Control Institute as a member.

Statutory ResponsibilitiesAPHIS regulates the importation of biologicalcontrol macroorganisms into the United Statesand their movement between states under theFederal Plant Pest Act3 and the Plant QuarantineAct4 (box 4-5) (360). Reliance on these plantpest statutes for jurisdiction often puts APHIS inthe position of having to justify its interven-tion—or avoid action altogether—in matters ofdirect import to the use of biological controlagents. Ongoing jurisdictional questions concernthe granting of permits for release to the environ-ment because the acts only cover the movementof agents; the control of “beneficial” organismsthat are not generally considered “plant pests” or“noxious weeds” yet may indirectly cause harm-ful impacts; and the labeling and quality controlof natural enemies. In addition, the statutesappear to suggest a zero-risk standard for intro-ductions of biological control agents—a standardthat is unrealistic and provides APHIS with littleguidance.

Jurisdictional uncertainties arise also in thecase of microbial pesticides based on nematodes.In accordance with the Federal Plant Pest Act,APHIS regulates the introduction and movementof nematodes in the United States. In light ofAPHIS’s official role, EPA retains no jurisdic-tion over these products; the Federal Insecticide,Fungicide and Rodenticide Act authorizes theagency to exempt pest control products that are

3 7 U.S.C. §147a et seq. (1957).4 7 U.S.C. §151 et seq.; 46 U.S.C. §103 et seq. (1967).

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BOX 4-4: The Proposed APHIS Regulation for the Introduction of Nonindigenous Organisms

USDA’s Animal and Plant Health Inspection Service (APHIS) currently grants permits for biologicalcontrol agents under regulations that cover plant pests. Scientists and natural enemy companies have

criticized APHIS’s approach for years because it lumps “beneficial” natural enemies into the same cate-gory with agricultural pests. In 1992 the agency’s Administrator instructed APHIS’s National Biological

Control Institute to meet with interested stakeholder groups to develop background information thatwould help in constructing a regulation more specific to biological control. But such a regulation never

appeared.

Instead, in January 1995, APHIS published a much broader proposed rule that applied generally to

nonindigenous species and superseded the agency’s earlier development of a biological control rule.The proposed regulation was APHIS’s attempt to address problems identified in the 1993 OTA assess-

ment Harmful Nonindigenous Species in the United States. That report summarized the harmful economicand environmental impacts of organisms that enter the country or spread and then become agricultural

pests, degrade parks and federal lands, or displace native species. The OTA report further specified thatthe piecemeal federal system for screening the importation or release of nonindigenous organisms con-

tributed significantly to these continuing harmful impacts.

Unfortunately, APHIS’s proposed rule did not do a good job of regulating both biological control (an

area that is actively promoted by the agency and has little firm documentation of past harmful impacts)and other types of potentially harmful introductions. Furthermore, the agency’s abandonment of its effort

to write a regulation specifically addressing biological control aroused the ire of scientists and industrymembers who had participated in the earlier process. Such feelings were only compounded by the

implied challenge in the rule to the deeply felt belief among many members of the biological control com-munity that theirs is a benign practice with little if any potential for causing harmful environmental impacts.

Response to the nonindigenous organism regulation was swift and almost uniformly negative.Responses could be tracked by interested observers via an Internet listserver constructed solely for this

purpose. A total of 252 responses came from biological control researchers, producers, practitioners,and distributors; university entomologists; farmers; weed control committees and districts; local, state

and federal agencies; members of Congress; commercial laboratories; and industry associations. Mostobjected to how the regulation categorized biological control along with other potentially harmful intro-

ductions. Many also felt that the permit requirements would place unacceptable financial burdens andtime constraints on the natural enemy industry, which already operates with a low profit margin.

Although most respondents expressed similar sentiments, they did not necessarily reflect an unbiasedsampling of expert or public opinion. The vast majority were in some way affiliated with the practice of

biological control, and the content of the regulation had been rapidly communicated throughout thisgroup by way of several listservers and bulletin boards on the Internet. Jeffrey Lockwood, a scientist

known for his concern about the potential ecological risks of biological control, was one of the few toexpress the opinion that the regulation was not strict enough. This view might have been better repre-

sented had other groups, such as conservation biologists, known about the regulation.

SOURCE: Office of Technology Assessment, U.S. Congress, 1995.

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adequately regulated by other federal agencies.Although APHIS claims to regulate these prod-ucts, and indeed the agency has processed a fewnematode applications over the years, in practicemost of these products go unregulated. Majornematode production companies contacted byOTA said they neither apply for APHIS permitsnor interact with the agency in any other way.Among the states, moreover, only Hawaii con-trols the entry of incoming nematode products,which are allowed into the state only under spe-cific research permits for greenhouse trials.Hawaii is evaluating nematode products in lightof the state’s long history of ecological harm bynonindigenous species (209).

The lack of oversight concerning nematodeshas had benefits as well as potential drawbacks.It has contributed to the nematode industry’s suc-cess in getting products on the market, particu-larly in light of the very low profit margins.What limited information has been generatedabout these organisms suggests that they are rela-tively innocuous and unlikely to cause harmfulenvironmental impacts. At the same time, how-ever, the taxonomy of these organisms is poorlyunderstood; some are ubiquitous in nature; and

many have a relatively broad host range. It isunclear whether the advantages from regulatingnematodes would outweigh the costs, but thismatter deserves more explicit deliberation andresolution.

APHIS proposed the Plant Protection Act andthe Animal Health Protection Act in 1990 andagain in 1995 to consolidate the provisions from28 statutes under two laws (144). Although theydo not completely resolve the mismatch betweenstatutory authority and regulatory needs, thesebills take steps to clarify certain jurisdictionalquestions. Specifically, the recently proposedPlant Protection Act adds to the definition of“plant pest” vertebrate and invertebrate animals,biological control organisms, and undesirableplant species (358). This last term replaces “nox-ious weeds,” liberalizing current noxious weedlaws by enabling port inspectors to quarantineunlisted plants even if those plants are not new toor widely prevalent in the United States. The lawdoes not define “biological control organism,”but leaves this term to be decided at a later dateby rulemaking with public input (144).

BOX 4-5: Pest Control Acts

■ The Federal Plant Pest Act of 1957 prohibits the movement of any plant pest from a foreign countryinto or through the United States without a permit from USDA. The definition of plant pest includes any

living stage of “any insects, mites, nematodes, slugs, snails, protozoa, or other invertebrate animals,bacteria, fungi, other parasitic plants or reproductive parts thereof, viruses, or any organisms similar to

or allied with any of the foregoing, or any infectious substances, which can directly or indirectly injureor cause disease or damage in any plants or parts thereof, or any processed, manufactured, or other

products of plants.” [7 U.S.C. §§150 aa et seq. (1957)].

■ The Plant Quarantine Act of 1912 bars the entry into the United States, without a permit, of any nurs-ery stock—and under certain conditions, any other class of plants, fruits, vegetables, roots, bulbs,

seeds, or other plant products—in order to prevent the introduction of any tree, plant, or fruit diseaseor any injurious insect not widely prevalent in the United States. The act also authorizes the Secretary

of Agriculture to forbid importation of plants from particular areas and to quarantine any U.S. localitiesto prevent the spread of a dangerous plant disease or insect infestation. [7 U.S.C. §§151 et seq.

(1967)].

SOURCE: Office of Technology Assessment, U.S. Congress, 1995.

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APHIS’s Permit SystemThe Plant Protection and Quarantine (PPQ) divi-sion serves as APHIS’s principal regulator ofbiological control agents. Through its permittingsystem, PPQ seeks to protect U.S. agriculturefrom the introduction and interstate dispersal ofharmful plant pests. APHIS includes biologicalcontrol agents among these regulated pests, asource of contention because arguably most ben-eficial natural enemies do not fit that character-ization. Enforcement by PPQ takes place atmajor U.S. ports of entry, while permitting is car-ried out by APHIS headquarters in consultationwith the states.

PPQ grants several thousand permits eachyear for introduction and interstate movement ofpathogens, invertebrate animals, and weeds. Pin-ning down exact information about types andnumbers of permits for biological control andlevel of technical review is difficult; in responseto OTA’s inquiry regarding numbers of applica-tions evaluated by agency entomologists eachyear, for example, APHIS supplied figures rang-ing from eight to 2,500 applications. In truth,most of the applications are processed by clericalstaff, but the inconsistency of information sup-plied to OTA illustrates APHIS’s recordkeepingproblems and raises questions about its sense ofaccountability.

It appears that most of the first-time (“unprec-edented”) applications are reviewed either byone of APHIS’s two entomologists or by theagency’s plant pathologist. Each year these sci-entists evaluate about 10 (and sometimes asmany as 20) applications for phytophagous(plant-eating) biological control organisms and aroughly comparable number for entomophagous(insect-eating) agents. Numbers of unprece-dented applications appear higher in 1995 than insome of the previous years (143). Each applica-tion is usually reviewed by one scientist, whoconsults occasionally with colleagues whenquestions arise.

PPQ has no process by which to expedite thepermitting of unprecedented, taxonomicallypromising species over those that may carryheightened capacity for ecological harm (such as

organisms that attack a wide range of nontargetplants and animals). Rather, APHIS categorizesapplications in accordance with the purpose ofthe introduction (movement or release), thepurity of the organism, and, eventually, the out-come of the environmental assessment. Datarequirements vary depending on whether theorganism is to be imported from another countryinto quarantine, moved between containmentfacilities, or released to the environment (box 4-6). APHIS plans soon to address some of OTA’sconcerns about setting priorities; in particular,the agency is posting on the World Wide Weband APHIS gopher a list of arthropods com-monly used for biological control of pest arthro-pods for which permits will be expedited (360).

Unprecedented releases of biological controlorganisms require the preparation of an environ-mental assessment. As part of this process,APHIS’s Biological Assessment and TaxonomicSupport (BATS) division is required to deter-mine whether the candidate control agent “mayaffect” endangered or threatened species. Some-times BATS contacts FWS, although someobservers suggest that communication and coor-dination between the two agencies is not alwaysadequate.

Some researchers have complained that issuesregarding endangered and threatened species donot enter early enough into the decisionmakingprocess. When they were about to release theirtest organisms, researchers at the University ofCalifornia had their APHIS permits challengedby local FWS field officers, leading to long,costly and counterproductive delays (24).Another example involved APHIS’s evaluationof permits for five types of insects to be used forthe control of purple loosestrife (two beetles toeat the flowers, two to eat the leaves, and oneroot weevil). APHIS approached FWS concern-ing three of these agents in June 1995, just twoweeks before the intended release date. APHISwas completing the final stages of its assessment,and the beetles were unlikely to survive muchlonger, putting FWS in the difficult position ofhaving to confirm, on very short notice, the intro-duction of biological control agents against a

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high-priority pest of natural areas. FWS scien-tists had many concerns, including possibleeffects on endangered or threatened nontargetspecies; the beetles’ lack of native natural ene-mies, and the fact that, once released, the beetleswould not be readily controllable. In July 1995,FWS acceded to the release of the beetles.APHIS’s handling of these situations, however,raises questions about the timely incorporation ofthreatened and endangered species issues into thepermitting process and the adequacy of coordina-tion with FWS.

According to members of the natural enemyindustry, much of the permitting processinvolves redundancy, delay, and unnecessarypaperwork at both state and federal levels. Manyof the permit applications are precedented, whichmeans they concern the same biological controlorganism that was granted a permit previously,coming from the same state or country of origin,imported under the same conditions, and based

on the same permit conditions and facilities.Often these repeated releases have been takingplace for 10 or 20 years. According to the Asso-ciation of Natural Bio-control Producers, a dis-tributor selling 20 different products tocustomers in 40 states would need 800 permitswhich would have to be reviewed every twoyears (11). APHIS has somewhat simplified theapproval process for pure cultures of precedentedorganisms, but further streamlining or permitwaivers may be warranted.

Rather than waste time and resources renew-ing old permits, critics contend that APHIS needsa tiered, risk-based system with built-in waiversfor repeated biological control releases, so thatthe agency can concentrate on the more high riskagents. Greater scrutiny may also be called forwhen the previous release has not become self-sustaining and was cleared before the agencyinstituted its data requirements (299).

BOX 4-6: Categories of Pest Organisms

APHIS divides permit applications into categories as follows:■ A—Foreign plant pests new to or not widely distributed in the United States; domestic plant pests of

limited U.S. distribution, including program pests; state regulated pests; and exotic strains ofdomestic pests;

■ B—Biological control agents and pollinators;

B(1)—High risk: weed antagonists; shipments accompanied by prohibited plant material or Cate-

gory A pests;

B(2)—Low risk: pure cultures of known beneficial organisms; and■ C—Domestic pests that have attained their ecological range, nonpest organisms and other organ-

isms for which courtesy permits may be issued.

All biologically-based pest control agents fall under category B, biological control agents and pollina-tors. APHIS has yet to examine the environmental impacts of organisms in subcategory B(1). Some of the

B(1) organisms may include hyperparasites or other impurities; they may come from a particular strainnever before introduced or from a new field site. Those organisms designated in subcategory B(2) are

pure cultures that have been cleared for release to the environment; most of these have undergone someform of environmental assessment or administrative determination. Some were previously imported into

quarantine as subcategory B(1) organisms.

SOURCES: D. Knott, Plant Protection and Quarantine, Animal and Plant Health Inspection Service, U.S. Department of Agricul-ture, Riverdale, MD, personal communication, May 4, 1995 and August 2, 1995; M. Royer, Biological Assessment and TaxonomicSupport, Animal and Plant Health Inspection Service, U.S. Department of Agriculture, Riverdale, MD, personal communication,April 20, 1995; U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Safeguard Guidelines For Contain-ment of Plant Pests Under Permit, June 1993.

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In response to such criticism of its permit pro-cess, APHIS says that the agency has many inno-vations under development. These include newinstruction sheets for preparing permit applica-tions and environmental assessments, a customersatisfaction questionnaire, guidelines for contain-ment facilities, optional electronic submission ofapplication data, and plans to formulate catego-ries of organisms excluded from permitting.APHIS hopes to offer some of these materials onthe Internet, and eventually to adopt a computer-ized system, enabling customers to track theprogress of their permit applications (360). Thesechanges might address some of the problemsidentified by OTA. APHIS should be com-mended on these planned initiatives and encour-aged to follow through with these improvements.

APHIS’s Data ReviewAPHIS began doing rudimentary environmentalassessments on biological control applications in1970, upon passage of the National Environmen-tal Policy Act. These early “administrative deter-minations” were often poorly documented andbased on incomplete information. The systemcontinued in place throughout the 1980s.

The new leaders at APHIS in the early 1990sinherited an arbitrary and nontransparent permit-ting system. In 1991 they revised the outline forprerelease environmental assessments. The newform requested much more extensive dataincluding host specificity, hyperparasites, threat-ened native species, and effects on natural ene-mies. In 1993, APHIS again rewrote itsrequirements for environmental releases. Thisso-called “NIDR” format, which continues in usetoday, asks for a detailed description of the pro-posed action, biology of the target (host) organ-ism and of the organism to be released (includingboth field and laboratory host range), status inNorth America, and expected environmental andhuman health impacts (359). While adding to thedata requirements, PPQ has tried to streamline itspermitting process in other ways, for example,

by granting genus-level permits for Aphytis (Sep-tember 1994), Encarsia (February 1995) andEretmocerus (April 1995).

APHIS’s review of applications for insect-feeding (entomophagous) biological controlorganisms has been particularly lax; APHIS hadvirtually no data requirements for such agentsuntil 1991. Even today, the agency is strugglingto develop scientific protocols for testing hostspecificity and other characteristics of the ento-mophagous agents. APHIS’s environmentalassessment for Scelio parvicornis, in April 1994,was considered a milestone in denying a permitfor an entomophagous agent (299).

Technical Advisory GroupAPHIS has a Technical Advisory Group on theIntroduction of Biological Control Agents ofWeeds (TAG) but lacks a similar body for bio-logical control of insects. This independent vol-untary committee was formed in 1957 primarilyto provide advice to researchers. Today, TAGreviews applications for biological control ofweeds and advises PPQ on whether to grant per-mission for quarantine or release.

Chaired by a member of the U.S. Army Corpsof Engineers, TAG has up to 16 members, half ofthem from USDA and the U.S. Department ofInterior (box 4-7). Usually TAG convenes with-out complete participation; only about five tonine representatives consistently participate inTAG recommendations (360,51,299). No partic-ular number constitutes a quorum. Although for-eigners are barred from voting, the Canadianreviewers participate actively, and there is inter-est in making them voting members (51).According to APHIS representatives, however,the Federal Advisory Committee Act5 prohibitsvoting membership by nonfederal members onfederal advisory committees like TAG. In fact,federal advisory committees can have nonfederalmembers so long as they follow the Act’s proce-dural requirements, such as announcement ofmeetings in the Federal Register and formal

5 Federal Advisory Committee Act, title 5, U.S.C.A., appendix 2, subsections 1-15 (1972), as amended.

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recording of meeting minutes. Thus, any deci-sion to restrict TAG membership to federal agen-cies should carefully weigh the desirability ofbroader representation against whatever coststhese procedural requirements impose.

When PPQ receives petitions for the biologi-cal control of weeds, it sends them to the TAGsecretary, who distributes them to the TAG rep-resentatives for comment. TAG reviews oftentake about three to four months because ofscheduling difficulties of the TAG representa-tives. TAG conducts most of its business by

mail; an annual meeting provides a forum toresolve controversial issues and to meet withweed control researchers. TAG is funded bymember agencies, with APHIS paying only forthe nongovernmental participation (51).

Although TAG is set up in an informal advi-sory capacity, in practice PPQ virtually alwaysfollows TAG’s recommendations. Formally,PPQ makes the final decision, however, as isrequired by the Federal Advisory CommitteeAct. TAG reviews only about 10 petitions annu-ally (50). Apparently this represents all of the

BOX 4-7: Technical Advisory Group on the Introduction of Biological Control Agents of Weeds

Membership of TAG Committee

U.S. Army Corps of Engineers, Chair

U.S. Department of Agriculture:■ Animal and Plant Health Inspection Service■ Agricultural Research Service

■ Cooperative State Research, Education and Extension Service■ Forest Service

U.S. Department of Interior:■ Bureau of Land Management■ Bureau of Reclamation

■ Fish and Wildlife Service■ National Park Service

U.S. Environmental Protection Agency

Weed Science Society of America

National Plant Board

Members-at-Large■ Canada (nonvoting)■ Mexico (nonvoting)

Executive Secretary: (APHIS/PPQ employee)

Reviews by TAG

From 1987 through 1994, TAG reviewed 86 petitions for release or quarantine of organisms. Annualtallies varied from a high of 19 in 1989 to a low of seven in 1993. There were 71 different agents (some

went through TAG as applications for quarantine and again for release) petitioned on 28 target plant spe-cies, mostly rangeland weeds. Four of the targets, leafy spurge (Euphorbia escula), diffuse knapweed

(Centaurea diffusa), spotted knapweed, and yellow starthistle (Centaurea solstitialis), accounted for 43percent of these petitions. Some 77 percent of the petitions received favorable recommendations from

TAG.

SOURCE: A. Cofrancesco, U.S. Army Corps of Engineers, Vicksburg, MS, letter to the Office of Technology Assessment, U.S.Congress, Washington, DC, May 12, 1995; U.S. Department of Agriculture, Animal and Plant Health Inspection Service, “Charterfor the Technical Advisory Group on the Introduction of Biological Control Agents of Weeds,” unpublished draft guidelines, 1990.

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unprecedented petitions received by APHIS eachyear for biological control of weeds. Pre-quaran-tine review is less stringent than that for releasebut enables TAG to advise and monitor biologi-cal control activities in the early stages of devel-opment rather than first confronting petitionersyears into their research (51). Pre-quarantinereview is done only if requested by a researcher(366).

Despite the fact that the representatives oftenconsult with outside sources (51), critics chargethat TAG lacks scientific expertise, particularlyin plant taxonomy, pathology, ecology and evo-lution (58). Another complaint is that, as strongproponents of biological control technologies,TAG members traditionally have disregardedsome of the negative repercussions of biologicalcontrol introductions. For example, TAG reviewmay not always screen against harmful impactson abundant species of native plants.

Although PPQ follows the TAG recommenda-tions, TAG does not use the exact data require-ments developed by PPQ. Nevertheless, PPQgenerally accepts the TAG decision in lieu of itsown data requirements (299). In the early 1980sTAG informally issued to researchers its owninternal guidelines, which differed from the PPQrequirements in some important ways. TAGasked petitioners to submit, for example, “dollarfigures concerning crop or other losses caused bythe weed and costs of its control, versus, if appli-cable, dollar figures concerning its beneficialqualities” (177), something never required byPPQ. TAG no longer requests such informationfrom petitioners. Nonetheless, researchers com-monly submit economic data, which is then con-sidered by TAG in its deliberations (51).

TAG has discontinued its use of publisheddata requirements. Instead, the group has looseguidelines indicating its main areas of review:

■ taxonomy of the target weed;■ test plant list;■ host-range testing and impact on nontargets;■ taxonomy of the agent;■ biology of the agent; and■ other issues raised by the researchers.

These guidelines and other information aboutTAG are not available to researchers in printedform, although experts in the biological controlof weeds generally know what TAG expects. Amore formal review document could helpresearchers gauge where to focus their attentionand resources. TAG recognizes this problem andis awaiting the development of a final rule byPPQ. At that time TAG will review the incomingPPQ applications for biological control of weeds.

Proposed RuleAs mentioned earlier, APHIS’s proposed rule onthe introduction of nonindigenous organismsencountered widespread criticism and eventu-ally was withdrawn. Although biological controlpractitioners considered the proposal heavy-handed, conservation biologists applauded cer-tain of its provisions.

Compared with current protocols, the pro-posed rule paid more explicit attention to geneticvariation in the control organism, recognizingthat different genotypes may require independentassessment of their potential for ecological harm.Rather than focusing solely on weeds, the pro-posal called for the careful appraisal of biologi-cal control agents of arthropod pests. In addition,it recognized that there are potential hazardsfrom movement of control organisms betweendifferent biogeographic regions of the UnitedStates. Finally, the proposal acknowledged that acontrol agent can harm a nontarget organism notonly by eating or parasitizing it, but also by inter-acting via intermediate organisms (219).

Although many of the data elements in theproposal have been required on a more informalbasis since 1991, the proposal extended theagency’s regulatory control in a number ofrealms. Its broad definition of nonindigenousorganism included any organism proposed forintroduction into an area of the United Statesbeyond its established range. Its list of speciessubject to the rule included organisms whichhave long been in widespread use as biologicalcontrol agents throughout the United States.

The proposed rule combined an odd mix ofmanagement approaches. On one extreme was

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the micromanagement of such features as thethickness of plastic bags (0.1270 millimeters) forseeds, the particular taxonomic groups listed tobe regulated, and specifications for the submis-sion of samples to three museums. Other provi-sions, however, suggested a much looser, morefluid approach to APHIS’s regulatory oversightresponsibilities; examples are the lack of clearstandards on purity; the lack of specific protocolsfor host-specificity testing, and the absence ofany reference to pre- and postrelease monitoringof nontarget effects.

That the proposed regulation failed to incor-porate any provisions for postrelease monitoring,even for higher risk releases, suggests a possiblereluctance by APHIS to confront the impacts ofits permitting activities. Over time, without anymonitoring, standards for successive applicationscannot benefit from knowledge gained about theimpact of prior releases (235). Until now PPQdid not even maintain in a usable form the basicrecords and databases on past releases. The PPQform 526 database was unable to locate prece-dented permitting decisions except by the appli-cant’s name (299). The computerized NIDRsystem instituted in early 1994 for environmentalassessment data was redesigned in summer 1995to enable PPQ to locate precedented permittingdecisions by organism (360).

❚ Environmental Protection AgencyIn the early 1980s EPA developed special datarequirements for biologically based products, butnot until fall 1994 did the agency separate out itsregulatory review of microbial pesticides andbiochemicals from that for conventional chemi-cal pesticides.

Today the regulated community generallygives EPA high marks for its actions on the reg-istration of microbial pesticides and pheromones.

The new Biopesticides and Pollution PreventionDivision (BPPD) has consolidated the agency’sBBT-related activities, streamlined the datarequirements, and provided registrants withfaster, less costly, more accommodating registra-tion services. Critics charge, however, that theagency is waiving too many environmental datarequirements and should pay closer attention tothe effects on ecosystems and on insects andother nontarget organisms. EPA’s protocols forhost-specificity testing, moreover, focus almostentirely on commercial species such as agricul-tural crops and honeybees, with little regard fornative organisms. Finally, a major challenge liesahead for the agency as genetically engineeredmicrobial pesticides raise unprecedented riskconsiderations that may require different regula-tory approaches.

Statutory ResponsibilitiesAlthough EPA oversees the use of pesticidesmarketed in the United States, the agency hasexempted from its jurisdiction all BBTs exceptthose derived from microbes used in pesticideformulations (e.g., bacteria, algae, fungi, viruses,and protozoans) or biochemicals (including pher-omones). A further exemption covers phero-mones used in traps. BBTs remaining withinEPA’s jurisdiction are shown in table 4-2.

This arrangement derives from section 25(b)of the Federal Insecticide, Fungicide and Roden-ticide Act, which authorizes EPA to exempt pes-ticides that are adequately regulated by otherfederal agencies or are of a character not requir-ing regulation under FIFRA6. Detailed testingprotocols to accompany the regulatory require-ments listed in 40 CFR Part 158 have beenspelled out by EPA in its nonregulatory PesticideTesting Guidelines, Subdivision M (393,394).7

6 In 40 CFR Part 152, Subpart B, EPA exempts all BBTs except eucaryotic and procaryotic microorganisms (cellular organisms with andwithout a distinct nucleus, respectively) and viruses.

7 Biologically based pesticides are also regulated under the food additive provisions of the Federal Food, Drug and Cosmetic Act(FFDCA). Section 402 designates as adulterated any food or feed that contains residues of any pest control agent unless such residue is cov-ered by a tolerance under sections 408 or 409 or an exemption from tolerance. To date, however, all microbial pesticides and most biochem-ical pesticides registered for use on food crops have been exempted from the requirement of a tolerance (223).

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Biopesticides and Pollution Prevention DivisionWithin EPA’s Office of Pesticide Programs,BPPD coordinates the registration, develop-ment, and promotion of biologically based pesti-cides. Formed in November 1994, BPPD aims toexpedite the registration process for microbialand biochemical pest control products, serve asan advocate for the use of safer pesticides, andfacilitate cooperative programs with state andfederal agencies, universities, and agriculturalgroups. In creating BPPD, EPA brought togetherfrom other divisions scientists experienced withthe evaluation and registration of biologicallybased products. BPPD has established two multi-disciplinary teams whose staffs work together ina shared office and are authorized to skip someof the many bureaucratic steps that normally addweeks to the registration process of pest controlproducts (402).

Although BPPD was created as a one-yearpilot division, the White House recentlyapproved EPA’s decision to make BPPD a per-manent division. The division is serving as themodel for the restructuring of the Office of Pesti-cide Programs as a whole. It illustrates theadvantages of bringing together into a singlegroup those responsible for the multiple scien-tific and regulatory steps in the registration pro-

cess. By speeding the availability of pesticidealternatives, BPPD could play a key role in theClinton Administration’s current initiative toexpand use of integrated pest management andreduce reliance on conventional pesticides.

As of April 27, 1995, EPA had registered 43biochemicals (mostly pheromones) and 45microbial pesticides (more than half of them bac-teria). Seven of these were registered by BPPD inits first six months of operation, and the othersby the Office of Pesticide Programs in presentand past years. According to BPPD, its turn-around time for registering pheromones andother biochemicals is 30 to 50 percent less thanthe time required by other EPA divisions forequivalent processing (47). Whether the registra-tion of microbial pesticides will be similarlyexpedited remains unclear. In general the regis-tration of microbial pesticides is much faster thanthat of chemicals because of substantially differ-ent data requirements and frequent use of datawaivers.

Like the new administrators in APHIS’s PPQdivision, EPA’s BPPD staff have inherited a dif-ficult recordkeeping task. EPA’s prior decisionsare scattered among multiple offices in a varietyof formats. At the same time, only rarely doesEPA require pre- and postrelease monitoring ofeffects on nontarget organisms (305). This fail-ure to evaluate impacts, combined with the chal-lenge of consistent recordkeeping, suggests thatthe agency may not adequately build on pastdecisions and learn from prior mistakes. Thisshortcoming will become increasingly importantas the number of BBT products submitted forregistration grows. Rather than require that regis-trants take affirmative steps to evaluate impacts,EPA relies on FIFRA section 6(a)(2), whichstates that if pesticide registrants come acrossinformation on unreasonable adverse effects,they must submit that information to EPA. Thisdirective may sometimes prove counterproduc-tive: Legally bound to notify EPA of negativeresults, producers may be disinclined to thor-oughly investigate risks from registered prod-ucts.

TABLE 4-2: Categories Regulated by EPA

Microbial pesticides

Natural and engineered:■ Algaea

■ Bacteriaa

■ Fungia

■ Protozoansa

■ Virusesa

Biochemical products

■ Enzymes■ Hormones

■ Natural plant and insect regulators

■ Semiochemicals (including pheromones)a

a These categories are included in OTA’s scope of BBTs.

SOURCE: Office of Technology Assessment, U.S. Congress, 1995.

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Registration RequirementsBPPD is working to revise and update EPA’sdata requirements for microbial pesticides andbiochemicals. The agency first developed its pes-ticide testing guidelines for “biorational” pesti-cides in 1982; those guidelines were rewritten forthe microbial products in 1989. Guidelines forthe biochemicals remain outdated and not inkeeping with current EPA practices.

Producers of microbial pesticides and phero-mones contend that compliance with the fullproduct testing requirements can be prohibitivelyexpensive. Although costs of testing are muchlower than those for chemical pesticides, the rev-enue generated by BBTs is much smaller as well.BPPD waives many tests, however, and some-times some of its fees. To fully test and register aBBT today costs between several hundred dol-lars and a half-million dollars. EPA’s annualmaintenance fees are $700 for the first productand $1,400 for subsequent products; the maxi-mum limits or “caps” on the total annual mainte-nance fees payable by any registrant are usuallybetween $55,000 and $95,000 (less for smallbusinesses) (404). Tolerance fees for food-useBBTs generally range from $20,000 to $25,000,most of which is refunded if EPA grants anexemption (274).

BPPD has been seriously investigating thepossibility of waiving both the maintenance andthe tolerance fees for microbial pesticides andpheromones. The laws currently allow EPA toreduce or waive these fees for minor crop regis-trations where the fee is likely to significantlyaffect the availability of the pesticide. EPA hopesthat the elimination of fees for BBT registrationwill spark an increase in applications (274).

BPPD calls for a customized data package foreach active ingredient registered, based on amulti-tier system of data requirements; in con-trast, a full set of data are usually required forconventional pesticides (217). EPA requiresapproval also for all large-scale field tests (morethan 10 acres, or 250 acres for certain phero-mones) of BBTs. In addition, the agency requiresnotification before small-scale field testing ofgenetically engineered organisms.

EPA requires registrants to submit data onefficacy for pesticide products used to controlpests that threaten the public health (e.g., dis-ease-carrying mosquitoes). The agency retainsauthority to order additional data where neces-sary. Some of the data are only conditionallyrequired; others are waived in specific circum-stances. For example, the use of microbial prod-ucts in packinghouses and other indoor spacescommonly triggers an exemption to the nontargettesting requirements because no outdoor expo-sure is expected (224).

Pheromones and other biochemicalsEPA is about to publish in the Federal Registernew exemptions for pheromone products. Allstraight-chained lepidopteran pheromones,regardless of application mode, are now exemptfrom the requirement of a tolerance and mayundergo field testing on up to 250 acres withoutan experimental use permit. Past testing on smallfield plots has been extremely difficult becauseof the high volatility and specificity of the phero-mones. This measure allows for testing of broad-cast and sprayable applications of pheromoneproducts over a wide area. Similar regulatoryrelief measures were provided earlier for allarthropod pheromones in polymeric dispensers(274).

Registrants of pheromones and other bio-chemicals must submit data on product identity,analysis, and manufacture; chemical residues;toxicology, and impacts on nontarget organisms(389). Often EPA waives most of these require-ments. As in the case of microbial products, thetoxicology and nontarget organism data aretiered; if the initial testing yields significantadverse effects, additional data points are added(218). Testing only rarely moves to subsequenttiers (305). Moreover, in light of the low toxicityand minimal expected human exposure to phero-mone products, EPA, in 1986, waived certainrequirements for mammalian toxicology studieson pheromones (218).

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Microbial pesticidesTesting for microbial products covers the samegeneral areas: product analysis, toxicology, resi-due analysis on food crops, and ecologicaleffects. In calculating experimental dosage, reg-istrants must take into account that environmen-tal levels of the microbial agent and associatedtoxins often increase after application, at leasttemporarily—unlike environmental levels ofchemical pesticides, which decrease over time(394). Toxicology data are set forth in three tiers,but EPA has never required data beyond the firsttier (217), which involves short-term tests fortoxicity, infectivity, and pathogenicity. Ecologi-cal effects testing is tiered as well, with the firsttier consisting of maximum-dose, single-specieshazard testing on nontarget organisms (394). Forgenetically engineered microbes, similar data arerequired on both the complete microbial productand the inserted DNA construct (224).

Environmental EffectsEPA’s principles for review of microbial pesti-cides emphasize the importance of selecting sus-ceptible, nontarget species (including insects,plants, wildlife) when testing for host specificity(394). In its actual testing protocols, however,the agency points to the specific organisms to betested, chosen by EPA in part for their sensitivityto the test products (304) but mainly for theireconomic importance, commercial availability,laboratory experience with the organisms, andthe fact that researchers “know how to run agood experiment” with them (223,305,394). Thisapproach contrasts with the more unstructuredapproach employed by APHIS in its host-speci-ficity requirements. Although EPA officialsemphasize the flexibility of their system and theease with which data requirements may be addedor subtracted, the extra effort needed to designcustomized lists of nontarget species and todevelop new testing methods for these organisms

may well take a back seat to other agency priori-ties.

EPA focuses heavily on the effects on nontar-get agricultural crops, an approach developedwith APHIS for the 1982 Subdivision M report.8

The agency rationalizes that cultivated crops areuniquely vulnerable because they are monocul-tures, nonmobile (unlike birds and insects), andcommonly nonindigenous. Although such think-ing may have been fashionable 14 years ago, thepotential harmful impacts on nontarget insectsand other organisms have since come to beappreciated. Moreover, declines in native naturalenemies ultimately may affect agricultural plantsby enabling pest populations to grow.

A related concern focuses on the lack of eco-system testing for microbial and biochemicalproducts. EPA relies primarily on observedimpacts (such as unusual persistence in hostorgans) following administration to the isolatedtest organism of massive quantities (the “maxi-mum hazard dosage level”) of the pest controlagent. Such focused testing protocols have pro-cedural advantages, but they overlook the com-plexity of natural systems and the possibility forharmful ecological repercussions beyond thoseimmediately apparent from short-term laboratorytesting on isolated specimens. EPA is spending$1,224,000 in fiscal year 1995 researching eco-system approaches for testing effects of bio-chemicals and microbial pesticides.

Genetically Engineered ProductsBPPD deals with genetically engineered micro-bial pesticides on a case-by-case basis. Agencyreview resembles in most respects that for othermicrobial products but places increased attentionon exposure and effects on nontarget species(305).

8 Pesticide Assessment Guidelines, Subdivision M: Biorational Pesticides (1982) (393). This document provides guidance on developingdata on biochemical and microbial pest control agents. Many of the provisions are obsolete. EPA has rewritten subdivision M only for micro-bial pesticides (1989) (394).

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Recent developmentsThe first field testing of genetically engineeredproducts took place a decade ago with release ofthe “ice minus” variant of the bacteriumPseudomonas syringae, designed to prevent frostdamage on potatoes and strawberries (234).

To date, EPA has registered two types ofgenetically engineered microbial products, oneinvolving Bt genes inserted into Bt, and the otherinvolving Bt placed in a killed bacterium (305).Raven, registered in January 1995, is a strain ofBacillus thuringiensis kurstaki into which theEcogen Company has incorporated genes ofanother Bt strain. With respect to environmentalimplications, EPA views the product as an insig-nificant departure from standard Bt products, andhopes in the future to exempt from notificationrequirements similar Bt products with inserted Btgenes. The other products, registered in 1991,use Bt in killed Pseudomonas fluorescens. TheMycogen Corporation killed the Pseudomonas,which can survive in a wide range of conditions,to prevent it from spreading the Bt genes to newlocations. The killed bacterium protects fromultraviolet radiation the encapsulated Bt toxin,allowing for longer field persistence (239).EPA’s main concern is to ensure that all the bac-teria are dead; the agency requires the monitor-ing of every batch produced (305).

Other genetically engineered products areundergoing testing. For example, the agencyrecently approved the field testing of a geneti-cally engineered baculovirus containing aninserted scorpion toxin gene that facilitates afaster kill rate. The scorpion toxin used is only afraction of the full toxin and does not affectmammals. It may affect some Lepidoptera andother insects.

Notification requirementsEPA’s final rule for field testing of geneticallyengineered microbial agents, published in Sep-tember 1994, amends 40 CFR Part 172 to requirenotification of EPA, and preliminary data sub-mission, prior to small-scale environmental test-ing of microbial agents modified throughrecombinant DNA technology. The rule applies

also to nonindigenous microbial pesticides notacted on by USDA (390).

Some scientists criticize the rule for targetinggenetic modification techniques rather than high-risk organisms or outcomes. They argue that thenew molecular techniques that manipulate DNAand transfer genes are potentially even safer andmore precise and predictable than their tradi-tional counterparts. This view ignores the factthat many efforts to genetically engineer micro-bial pesticides have thus far focused on expand-ing target range, altering kill level and rate, andprolonging field persistence—characteristics thatcould affect environmental impacts in importantways. The critics also say that EPA should worryinstead about agents manipulated by othermeans, such as chemical or radiation mutagene-sis, transduction, transformation, or conjugation,which pose greater environmental risks andcould pollute waterways (234).

Other scientists counter that gene-splicingtechniques are a valid trigger for EPA review;elevated risks stem from the introduction of newliving forms that have never had an opportunityto evolve any checks and balances in nature. Sci-entists’ understanding of microbial communitiesand of the full import of particular species in thefunctioning of ecosystems is limited. Conse-quently, genetically engineered microbial pesti-cides may have wide-ranging consequences thatmay be difficult to evaluate (172).

Whatever the outcome of this debate, a pru-dent response by EPA requires scrutiny and flex-ibility, given the types of characteristics beingengineered into microbial products and the pau-city of information on potential environmentaleffects.

ResistanceOne of the most significant challenges facingBPPD is the prevention of resistance to Bt. Somescientists believe that large-scale squandering ofthis microbial pesticide may result from thewidespread use of crops engineered to containthe genes for Bt toxin. The use of these trans-genic plants is expected to create tremendousselection pressure among lepidopteran and other

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pest species, resulting in the rapid developmentof resistance to Bt. The susceptibility of Bt toresistance has already been documented, withearly evidence emerging from certain regions ofNew York, Florida, and Asia. Potential loss ofmicrobial Bt products poses a serious threat toagriculture in locations where pests have evolvedresistance to chemical controls. In parts of Mex-ico, for example, Bt products are among the onlyoptions left against the tomato pinworm; the pesthas become resistant to other pesticides (40).Campbell and other growers in that region relyon the availability of effective Bt-based pesti-cides.

Although EPA is working with manufacturersto develop strategies to manage resistance, it isunclear that any of these ad hoc attempts willactually work. Clearly, resistance has not beensuccessfully prevented in the case of chemicalpesticides (see chapter 2); EPA has no real trackrecord in this arena (156). Some scientists arguethat the effective management of resistance to Btwill require the concerted efforts of multiple par-ties. A recent article in Science, for example,urges development of a national research agenda,with full cooperation of industries, universities,and government, to develop and implement resis-tance management strategies for conventionallyapplied and transgenic Bt toxins (221).

To date, EPA has registered only transgenicpotato (May 1995) and field corn (August 1995),although other crops genetically engineered forpesticidal properties are coming through theresearch and registration pipeline (182,156). Aspart of the registration process for these products,EPA has developed cooperative agreements withproducers dealing with tactics to manage resis-tance (156,214).

Exactly how Monsanto will prevent the devel-opment of resistance to Bt from its potato prod-uct remains unclear; thus far, the company’sresistance management strategy includes fewclearly defined elements (402). In some respects,however, EPA views the Bt potato resistancemanagement activities as a test case: Inasmuchas Bt is only partially effective against the Colo-rado potato beetle, loss of the microbial pesticide

against this pest, hastened by its use in transgeniccrops, will not create a major new gap in the pestcontrol arsenal. Because the beetle has alreadydeveloped resistance to many chemical pesti-cides, however, it is important to try to prolongthe effectiveness of every control method avail-able.

Resistance management for Bt field corn—and eventually for transgenic sweet corn and cot-ton plants—will present greater challenges forEPA. The pests that feed on cotton and sweetcorn, and to a lesser extent on field corn, attack anumber of vegetable crops and ornamental plantsas well (404). Therefore, pest resistance inducedby large-scale use of Bt in transgenic cultivars ofthese crops may make ineffectual the use of Bt-based pesticides against pests that attack not onlycorn and cotton but also a range of other crops(156).

The resistance management plan for Bt fieldcorn includes: a Bt dosage meant to be highenough to kill all susceptible pests; annual moni-toring for development of resistance; farmer edu-cation programs; and, once use of Bt cornbecomes widespread in three to five years, therequired planting of non-Bt corn as a certain per-centage of acreage on each farm that uses Btcorn. The effectiveness of these approachesremains uncertain. EPA’s agreement requires theMycogen and Ciba-Geigy corporations to carryout research on many related issues; their resis-tance management strategies are likely to changeas new evidence emerges (404).

❚ Food and Drug AdministrationU.S. Food and Drug Administration (FDA), arelative newcomer to the regulation of BBTs, hasyet to identify exactly what roles it will play. Theagency may face increasing responsibilities inthe future, however, as BBTs become moreprominent in food-related industries and posthar-vest uses.

FDA has authority to regulate the BBT usesthat are not subject to EPA or USDA jurisdiction.To date, however, the agency has chosen only toadvise state and local health officials; to enforce

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grading standards for natural enemy and otherinsect fragments in stored grain; and to contem-plate possible oversight of the use of BBTs, spe-cifically, insects and nematodes in food serviceestablishments and other food-handling institu-tions.

FDA could assume a greater role if itdesired. It would need to designate EPA-exempted BBTs (i.e., natural enemies) as foodadditives in cases when the BBTs could becomea component of stored or prepared food andUSDA lacks regulatory jurisdiction. FDA couldthen establish and enforce tolerances for BBTsunder section 409 of the Federal Food, Drug andCosmetic Act (FFDCA). Although authorized todevelop standards for BBTs (195), however,FDA would prefer to remain responsible only forenforcement of the BBT-related regulations setby EPA.

Two recent controversies may help elucidateFDA’s current and future roles in regulatingBBTs.

Postharvest Grain StorageUntil 1993, FDA, EPA, and USDA struggled toresolve the question of which agency had statu-tory jurisdiction over BBTs used for postharvestgrain storage (195). Previously, EPA had prohib-ited such BBT use. Following extensive inter-agency discussion, FDA was chosen to shoulderthe responsibilities.

FDA has determined that nematodes and pred-atory and parasitic insects released into grainstorage areas for pest control purposes areunlikely to become a component of food. There-fore FDA, in conjunction with USDA’s FederalGrain Inspection Service, will continue gradinggrain according to the existing standards forwhole insects, fragments, parts and other resi-dues, without special requirements for BBTs (1).

In setting these maximum allowable levels,commonly referred to as defect action levels(DALs), FDA recognizes that some foods willcontain insects and insect parts at low levels thatare not hazardous to the consumer. FDA desig-nates as adulterated, however, those productsfound to exceed the DAL for insect fragments.

Adulterated products are seized by FDA and, ifthey cannot be cleaned by further processing,destroyed.

Food Service AreasThe release of parasitic and predatory insects andnematodes into food service establishments andfood-handling institutions has also created con-fusion over statutory jurisdiction. Unlike the con-troversy surrounding postharvest grain storage,this issue has been only partly resolved despiteextensive discussions among USDA, EPA, FDA,and members of Congress.

After 11 months of indecision, the agenciesdecided that neither EPA nor USDA would regu-late BBTs when used in food preparation areas.The task of how or whether to regulate BBTs forthese uses has been left to FDA. FDA, however,has no formal policy or procedure to date (147)and has not assumed responsibility for conditionsin restaurants and other institutions with foodpreparation areas (195). FDA restricts its activi-ties to the manufacturing side of food productsand leaves food preparation areas to state andlocal health officials. The agency issues recom-mendations, for the sake of uniformity, which thelocal and state offices can independently chooseto adopt. On the assumption that introducedinsects might find their way into food, puttingthe consumer at risk, FDA has recommendedagainst the use of insects and nematodes as a pestcontrol practice in food preparation areas (195).

The agency is now considering whether toregulate these insects and nematodes as foodadditives under section 409 of the FFDCA or toleave the decisions up to state health depart-ments. Under section 409 (104) any substancemust be an approved food additive or generallyrecognized as safe (GRAS) for its intended use,if its intended use results in its becoming a com-ponent of food. FDA does not consider theseinsects to be GRAS for their intended use andtherefore has the authority to regulate them asfood additives (148). It may decide to do so ifdata show that the insects may become a compo-nent of food.

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FDA is currently reviewing its position and iswilling to receive and review any valid datashowing that there is no reasonable expectationthat the insects will become a component of thefood (147). It is unclear what further action the

agency will take. In all probability, FDA will notassume a greater role unless forced to do so,enabling state or local health officials to maketheir own decisions (box 4-8).

BOX 4-8: Chronology of the Praxis Company’s Experience with FDA

For two years, Praxis Integrated Biological Cybernetics, a small company in Allegan, Michigan, has

been corresponding with local, state, and federal officials in hopes of obtaining permission to resume itsuse of parasitic wasps and nematodes for cockroach control in food service areas (restaurants, schools,

nursing homes). Despite congressional intervention on behalf of Praxis, an agreeable solution has comeonly with considerable difficulty, years of delay, and great expense to the company.

In 1993, a Detroit bakery solicited Praxis’s help in controlling cockroaches. Uncertain about regulatoryrequirements, the bakery contacted the Michigan Department of Public Health. Knowing little about these

natural enemy products but concerned about their potential effects, the department director prohibitedPraxis from any further releases of wasps and nematodes as of October 1993 and recommended that an

advisory group be assembled with representatives from EPA and USDA to determine the appropriateregulatory response.

Weary of the inability of state and local officials to come to a conclusion, Praxis’s owners sought the

help of their representative in the U.S. Congress, the Honorable Peter Hoekstra, who wrote to EPArequesting its assistance in resolving the issue. In response to Congressman Hoekstra’s letter, EPA

replied that while “EPA registers pesticides and regulates their use, parasites, predators, or macrobiolog-ical agents (including nematodes) are not required to be registered.” Because EPA considered these

organisms to fall under APHIS’s jurisdiction, EPA would not make a determination as to their safety. Con-gressman Hoekstra proceeded to contact both USDA and FDA requesting an expedited determination

on the safety of Praxis’s products.

In a letter to the Michigan Department of Public Health dated January 13, 1994, FDA stated that whileeating establishments are principally regulated by local and state agencies, FDA felt that the EPA exemp-

tion did not cover use in retail food establishments—thus implying that EPA was responsible for makingthe decision. The letter also stated that FDA would not recommend or condone the use of biological con-

trol agents in a public eating facility. The following month, USDA-APHIS responded to CongressmanHoekstra’s inquiry, concluding that APHIS, like EPA and FDA, was not responsible for regulating the bio-

logical control agents for these specific uses.

In March 1994, FDA reiterated its belief that EPA was responsible and that, if so requested, FDA would

assist EPA in making the determination. The contradictory agency responses prompted CongressmanHoekstra to request a telephone conference with the appropriate individuals at EPA, FDA, and USDA. In

May, Praxis was notified that these agencies were holding preliminary conferences to decide how to han-

dle the situation. By October 1994, however, neither Praxis nor Congressman Hoekstra had been con-tacted regarding a solution. Congressman Hoekstra sent a letter in October and a fax in December of

1994 expressing his concern about the delay.

In January of 1995, FDA responded to Praxis in a letter stating that “extensive discussions” had been

held to determine statutory authority. It was decided that neither EPA nor USDA-APHIS would regulate thewasps and nematodes. The letter concluded that FDA would be willing to review data supporting the

safety claims made by Praxis, but that any action on the part of FDA would not override regulatory actionsby the state or other local agencies.

(continued)

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REGULATING THE RISKS FROM BBTS: ISSUES AND OPTIONS

❚ Regulatory Structure for Natural Enemy Industry and Biological Control ResearchThe current regulatory system under APHIS hasa number of important flaws. Its requirementsand permitting process for the natural enemyindustry lack balance, transparency, and effi-ciency. Small companies must comply with oftenuseless paperwork and critical delays in shippingorganisms that have a long history of repeatedintroduction and widespread use.

Past permitting of classical biological controlintroductions by researchers has been uneven,with the greatest focus on biological controlagents targeting weeds, and relatively little scru-tiny of agents affecting insect pests. The exist-ence of an advisory group (TAG) only for weedsdemonstrates the varying levels of evaluation. Toimprove the agency’s regulatory decisionmak-

ing, APHIS needs to give more complete cover-age to all biological control introductions, and todevelop better documentation of nontargetimpacts from past introductions.

Significant environmental risk issues existthat APHIS needs to identify and evaluate. Theagency’s recently proposed (and subsequentlywithdrawn) regulation on the introduction ofnonindigenous species, however, was clear evi-dence that APHIS has not yet succeeded inassigning priorities and addressing these risks.The proposal was exceedingly stringent in someareas and overly lax in others.

Congress could, through its oversightfunctions, instruct APHIS to streamline its permittingprocess and to design a more balanced regulatorysystem for biological control. Components of thesechanges might include the following:

■ Developing a more even-handed regulationfor biological control with broader input from

Although frustrated by the 16-month delay, Praxis agreed to send FDA copies of information that hadpreviously been provided. Praxis’s owners made another request for the phone conference that had been

promised 10 months earlier. In February, after several delays, the phone conference was held. Praxis wasasked to provide additional data to enable FDA to determine the safety of the products. At the conclusion

of the meeting, FDA promised a final decision within 90 days.

The state of Michigan, meanwhile, convened an advisory group (Michigan Human Living Environment

Pest Management Advisory Group) in the summer of 1994 to examine possible human health risks and torecommend safety procedures for the indoor use of biological control agents. In the absence of an FDA

ruling, the group submitted its findings and recommendations in June of 1995. The group decided infavor of Praxis, resolving that the Michigan Department of Public Health should allow the use of biological

control agents in food service establishments as part of an IPM plan.

FDA’s final decision in August of 1995 also supported Praxis. FDA decided not to recommend that theState of Michigan prohibit Praxis from marketing parasitic wasps and nematodes for cockroach control.

Praxis is now free to move forward with its parasitic wasps and nematodes, but the two year delay has

considerably drained the company’s resources. The company continues to struggle to market its prod-ucts. According to Praxis representatives, Cooperative Extension agents and university scientists insist

that if the company wishes to gain their support, Praxis not only must submit to them proprietary informa-tion but also must allow them to publish that material. Convincing Extension Agents to recommend the

company’s biological control products—or at least not to dissuade potential customers—may prove to beanother uphill battle for Praxis.

Source: Office of Technology Assessment, 1995.

BOX 4-8: Chronology of the Praxis Company’s Experience with FDA (Cont’d.)

OPTION

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all stakeholders (researchers, natural enemycompanies, farmers and other users, wildlandmanagers, state agencies, conservation biolo-gists, etc.).

■ Formulating an explicit policy concerning theregulation of nematodes. Although formallywithin APHIS’s jurisdiction, nematode prod-ucts rarely go through APHIS review. Theagency needs to carefully consider whetherthis leaves any significant risk issues unad-dressed. Potential impacts on companies pro-ducing nematode-based products must weighinto the development of a more formal policy.

■ Instituting a technical advisory group (TAG)to evaluate proposed introductions of unprec-edented biological control agents targeted atinsect pests (entomophagous agents), andimproving the science underlying the regula-tory decisionmaking for these agents by devel-oping appropriate host-specificity testingprotocols. The different standards of reviewfor biological control agents targeting plantand insect pests are based on historical con-cerns about agricultural crop protection andignore our scientific understanding of theimportance of native biodiversity and thevalue to agriculture of conserving native natu-ral enemies. Enhanced review of entomopha-gous species may provoke objection fromentomologists who are not used to this level ofscrutiny.

■ Developing mechanisms through which to includeinput from a cross section of nongovernmentalorganizations, including those concerned withenvironmental risk and conservation issues, inAPHIS’s decisions about biological controlagents. The Federal Advisory Committee Actallows membership on advisory committees bynonfederal agencies so long as the committeesadhere to certain procedural requirements. IfAPHIS chooses not to expand TAG membership,other channels may be available for nonfederalinput.

■ Requiring post-release monitoring of the non-target impacts from the highest risk introduc-tions as a condition of the permitting process.The challenge is to develop a mechanism for

funding such research, so as not to placeundue burdens on a low-profit industry thatproduces a valuable set of low-risk pest con-trol tools.

■ Maintaining clearer records of permittedreleases, the basis for these decisions, and anysubsequent impacts, to improve future deci-sionmaking. According to APHIS, some ofthese changes are already in progress; theseefforts deserve support and encouragement.

■ Convening a panel of scientific experts toevaluate APHIS’s past regulatory precedentsas a basis for future permitting decisions. Thisreview could help APHIS identify some of thehigh-risk releases and facilitate agencystreamlining of other permitting activities.

An opportunity to address some of theflaws in APHIS’s regulatory system may present itselfin the agency’s efforts to consolidate all of its plantprotection statutes into a single package.

❚ EPA’s Regulation of Microbial Pesticides and Pheromone ProductsRecent actions by EPA’s Biopesticides and Pol-lution Prevention Division to expedite the per-mitting of pheromones and microbial pesticideshave received high marks by the regulated indus-try. The division’s strides in streamlining BBTregistrations will need to retain some balance inthe long run, especially regarding granting ofwaivers for environmental testing. Microbialproducts that have been genetically engineered tobehave like conventional pesticides (see chapters3 and 6) will need to be handled with care,because some will pose risks similar to thoseassociated with conventional pesticides ratherthan having the relatively benign environmentalprofile of microbial pesticides registered to date.

Congress could, either by amendmentto FIFRA or through its oversight functions, instructBPPD to pay closer attention to possible nontargetimpacts on native insects and other noneconomicspecies, and to begin considering how it will deal withmicrobes genetically engineered for broader spec-trum impacts and faster and higher kill rates. (Oneoption would be to pass these on to other EPA divi-

OPTION

OPTION

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sions to be dealt with as conventional pesticides, butsuch action could substantially thwart development ofgenetically engineered microbial pesticides byremoving the cost incentive to produce such prod-ucts—see chapter 6.)

❚ Consistency in the Regulatory StructureSome analysts have identified as an importantproblem the lack of consistency among APHIS,EPA, and FDA in the agencies’ regulatory over-sight of natural enemies and microbial pesticides.They suggest that both types of BBTs pose simi-lar questions of nontarget effects and other envi-ronmental risks (e.g., 235). They argue that thesetwo categories of BBTs need an overall regula-tory umbrella, a single law or a single agency togive microbial pesticides and natural enemiesequal coverage.

Congress could pass a new lawembracing uses of natural enemies and microbialpesticides that would give more similar coverage tothese two categories, but OTA does not find sufficientjustification for this option. EPA, FDA, and APHIS allhave expertise in different areas, which correspondsat least roughly with their current regulatory responsi-bilities. It is important, for example, that EPA continuetoxicity studies on certain microbial products; theother agencies are unequipped to take over that func-tion. Certainly regulatory gaps exist, but these can beaddressed within the current institutional framework(see previous options).

❚ Anticipating the Occurrence of Pest Resistance to BBTsScientists believe that resistance is probable forbacteria- and virus-based microbial pesticidesand possible for several other categories ofBBTs. The rates at which resistance appears arelikely to be slower than those for conventionalpesticides. Of particular concern, however, is thethreat of more rapid development of resistance toBt-based microbial pesticides from the antici-pated large-scale use of crop plants geneticallyengineered to contain the Bt toxin.

The problem of managing resistance toBt is exacerbated by the lack of clear understandingof its scientific underpinnings and the paucity of dem-onstrated successes in countering this phenomenon.EPA is requiring the development of resistance man-agement plans as a condition for its registrations ofBt-containing crops, but the effectiveness of theseprovisions remains uncertain. To prevent the loss ofthis valuable tool in the pest control arsenal, Congressmight consider funding research on mechanisms tohalt or reduce the development of resistance (e.g.,specific use patterns for the transgenic plants), possi-bly as part of a cost-sharing program with potentiallyimpacted commodity groups.

Recent deliberations in Congress have cen-tered on whether EPA should keep or transfer toAPHIS its regulatory oversight of plants geneti-cally engineered for pesticidal properties. OTAhas identified several technical and institutionalfactors that favor retention of jurisdiction byEPA. Crops that are manipulated to express theBt toxin raise many of the same issues (resis-tance, toxicology, etc.) that EPA has addressed inthe context of microbial pesticides. Only EPAhas the experience, scientific capacity and infra-structure with which to tackle these difficultproblems with any hope of success. Moreover,the agency has the necessary authority to desig-nate specific use patterns, labeling requirements,and training programs that could help preventresistance and thus the loss of Bt-based pest con-trol tools. APHIS lacks the relevant experienceand statutory authority to adequately address theBt resistance problem.

❚ Adjusting Regulatory Requirements for Chemical PesticidesIntegrated pest management (IPM) involves thecombined use of multiple pest controlapproaches. Conventional pesticides often areused in concert with augmentation or conserva-tion of natural enemies. However, many pesti-cides kill the natural enemies as well as the pests.Information on such effects could enable pesti-cide applicators to reduce or eliminate applica-tions of certain conventional pesticides to protectpopulations of natural enemies.

OPTION

OPTION

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Congress could amend the FederalInsecticide, Fungicide and Rodenticide Act to includeproduct labeling requirements that alert users to theimpacts of pesticides on populations of natural ene-mies. Currently, Germany requires that pesticidelabels indicate the level of harmfulness to beneficialarthropods. A U.S. system could incorporate similarprovisions. For example, a German label reads:

This product is ‘harmful’ for populations ofAphidius rhopalosiphi (parasitic wasp), ‘slightlyharmful’ for populations of Coccinella septem-punctata (ladybird beetle), ‘not harmful’ for pop-ulations of Poccilus cupreus (carabid beetle).

The species listed are chosen based on such factorsas sensitivity to the product and likelihood of expo-sure (106). Although no other countries presentlyrequire such a labeling system, the European Unionmay consider adopting a similar program as part of its

efforts to harmonize requirements. (For other regula-tory examples from abroad, see box 4-9.)

❚ Anticipating Food Safety IssuesPressures on FDA to play a role in BBT regula-tion will grow as applications of these technolo-gies to control postharvest diseases in food-related industries increase. Current ambiguityabout the agency’s role has had negative reper-cussions for at least one BBT company and itsclients, who need a more predictable and work-able system.

Congress could instruct FDA to analyzeand firm up its current and future role in this area. Inview of FDA’s recent experience with the state ofMichigan and the Praxis Company, a small invest-ment of resources into workshops or policy sessionsto review the important issues now would precludesignificant bureaucratic entanglements and theresources they consume down the line.

OPTION

OPTION

BOX 4-9: Other Regulatory Systems

The Australian Biological Control Act and the draft code of conduct of the United Nations’ Food and

Agriculture Organization (FAO) are often cited as regulatory models deserving consideration or emulationby policymakers in the United States. These systems are described here. Also included is the Interna-

tional Convention on Biological Diversity, which raises ownership issues that may affect future prospect-ing for biological control agents in other countries.

Regulation of BBTs Down Under

Australia relies on a combination of BBT-related laws. The Quarantine Act (1908) and the Wildlife Pro-tection Act (1984) control the importation of exotic organisms into quarantine and for release. The Genetic

Manipulation Advisory Committee, which lacks legal authority but wields considerable power regardless,oversees the release of genetically modified BBTs (a mandatory rule is under development). And the

National Registration Authority has responsibility for approving commercial biological pesticides such asBt, in addition to chemical products. The use of non-exotic organisms is not regulated unless they are

genetically modified or they merit examination in a manner similar to that of agricultural and veterinarychemicals. The Australians invoke their widely acclaimed Biological Control Act (1984) only as a last

resort, when the choice of a target or the use of a particular control agent is likely to be controversial. Todate, the act has been summoned only for two programs, controlling the annual weed Paterson’s curse

(Echium planatagineum) and the blackberry (Rubus fruticosus). In the latter case the use of the law wasthreatened but never executed.

(continued)

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Australia’s Biological Control Act is the only biological control legislation ever adopted by a nationalgovernment. Several features of the act deserve attention. First, the act directly addresses biological con-

trol, unlike laws in the United States which apply to BBTs only secondarily in the context of noxiousweeds, conventional pesticides, or other concerns. Second, compliance with the act is not mandatory. It

is there to be invoked only if needed. Third, the act places considerable emphasis on the inclusion of allissues and public comments, but where a decision to proceed is then made, the individuals or organiza-

tions involved are freed from liability. Fourth, although the Biological Control Act offers a valuable mecha-nism on certain occasions, it may be used only rarely in light of the substantial time and expenditure

involved. Fifth, in contrast to U.S. approaches, the Biological Control Act includes serious considerationof the target organism. When the Agriculture and Resource Management Council of Australia and New

Zealand recommends declaration of a target pest, the Biological Control Authority must publish its inten-tion in widely circulating newspapers and journals, giving relevant information and inviting comment. If

further information is needed, the Biological Control Authority may initiate an inquiry by the IndustriesCommission or under the Environmental Protection Act or a specially constituted body, depending on the

issues at stake. Decisions on individual biological control agents with which to control the target organismfollow much the same course, although publication in the Commonwealth Gazette (Federal Register) isdeemed sufficient.

FAO Draft Code of Conduct for the Import and Release of Biological Control Agents

The U.S. government is participating in the completion of the FAO code of conduct, a voluntary set of

standards for the importation of BBTs capable of self-replication—parasites, predators, nematode para-sites, plant-eating arthropods, and pathogens. The code will cover agents imported for research as well

as for field release, including those used in classical biological control and those packaged or formulatedas commercial products. The recommendations of the code do not distinguish between different kinds of

BBTs, in contrast to the U.S. regulatory approach which addresses separately biological control importa-tions and the use of microbial pesticides. Pheromones and resistant host plants fall outside the scope of

the code. Toxic products of microbes that are used as pesticides, which cannot reproduce and whichbehave like conventional pesticides, are covered instead by the International Code of Conduct on the

Distribution and Use of Pesticides (1990). In the future, the biological control code may apply also togenetically engineered BBTs.

The FAO code describes the responsibilities of governments and of importers and exporters of BBTs

before, during, and after importation. Its provisions include, for example, the designation by each govern-ment of a competent authority to oversee BBT imports and releases; the use of precautions against the

export of BBTs adulterated with their own natural enemies or with other contaminants; and the prepara-tion of dossiers on the pest to be controlled (to justify the importation of a control agent) and on the candi-

date biologically based control agent (to document its identity and potential human and environmentalrisks). The draft code emphasizes that every effort should be made to transport the BBT at a life-cycle

stage during which it can survive without its host pest (the entry of which could present an additionalquarantine risk). The code also stresses the importance of proper labeling, post-release monitoring, dep-

osition of voucher specimens, education and training of users, and other procedures.

(continued)

BOX 4-9: Other Regulatory Systems (Cont’d.)

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Chapter 4 Risks and Regulations | 107

Convention on Biological Diversity

The United States is a signatory to the Convention on Biological Diversity, an international agreement

promoting the conservation of biological diversity and the equitable sharing of benefits arising from theuse of genetic resources. The convention does not specifically mention biological control, but it touches

upon related issues such as the commitment of countries to control alien pests (Article 8.h) and the cre-ation of conditions facilitating access to genetic resources for environmentally sound uses (Article15.2).

Several countries, most notably China, India, Brazil and Mexico, have interpreted the convention to

suggest that the nation importing the biological control agents from abroad must reimburse the country oforigin. Article 15.7 calls for “sharing in a fair and equitable way the results of research and development

and the benefits arising from the commercial and other utilization of genetic resources with the Contract-ing Party providing such resources.” Article 19.2 addresses specifically the benefits arising from biotech-

nologies based upon genetic resources, and emphasizes developing countries’ special need for access.Article 15.1 acknowledges state sovereignty over resources: “...the authority to determine access to

genetic resources rests with the national governments and is subject to national legislation.” These pas-sages could imply the development of a fee system for the collection of natural enemies from abroad.

Undoubtedly this option is controversial, however, particularly because the pests themselves commonlyoriginate from those same countries and because the international exchange of natural enemies can be a

mutually beneficial enterprise.

At least 98 countries worldwide have been the source of biological control agents for one or more pro-grams, and 121 countries have introduced at least one agent. Countries in the developing world have

been the source of 57 percent of all biological control introductions against alien insect pests worldwideand the recipient of 52 percent of all such biological control introductions.

SOURCES: Office of Technology Assessment, U.S. Congress, 1995, compiled from Centre For Agriculture and Biosciences Inter-national, Using Biodiversity to Protect Biodiversity: Biological Control, Conservation and the Biodiversity Convention (Wallingford,Oxon, UK: 1994); J.M. Cullen and T.E. Bellas, Division of Entomology, CSIRO, Canberra, Australia, “Australian Laws, Policies andPrograms Related to Biologically-Based Technologies for Pest Control,” unpublished contractor report prepared for the Office ofTechnology Assessment, U.S. Congress, Washington, DC, March 1995; United Nations Environment Programme, Convention onBiological Diversity, June 5, 1992 (as of July 20, 1995: URL=gopher:\\Gopher.UNDP.Org:70/00/Unconfs/English/Biodiv.Txt, nodate); United Nations Food and Agriculture Organization, Draft Code of Conduct for the Import and Release of Biological ControlAgents (Rome, Italy: November 1994); J.K. Waage, Director, International Institute of Biological Control, Ascot Berks, UK, letter tothe Office of Technology Assessment, U.S. Congress, Washington, DC, July, 1995.

BOX 4-9: Other Regulatory Systems (Cont’d.)

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| 109

5From Research to

Implementation

he federal government plays a large rolein the research, development, and imple-mentation of biologically based technol-ogies for pest control (BBTs). At least

11 agencies are involved, and annual expendi-tures amount to over $210 million. Despite thesize of these efforts, BBTs do not move smoothlyfrom research to providing on-the-ground solu-tions to pest problems (see also chapter 3). Thischapter explores some of the reasons for thebottleneck. It begins by describing activities offederal agencies related to BBT research andimplementation and then examines how the fed-eral government influences decisions of farmersand other users to adopt BBTs. The chapter con-cludes by identifying a series of issues andoptions for improving the flow of research find-ings into their practical applications.

OVERVIEWSeveral federal agencies conduct or fund BBTresearch. Total funds allocated to BBTs by theseagencies exceed $160 million annually, approxi-mately $30 million of which comes from thestate matching funds through the CooperativeState Research, Education, and Extension Ser-vice (CSREES) (table 5-1). The states also make

substantial contributions directly to the StateAgricultural Experiment Stations and to landgrant universities.

The public sector spends approximately $90million each year on pest control programs basedon BBTs (table 5-2). Of this, about $10 millionrepresents the biological control programs run by28 state departments of agriculture. The preciseamount that goes toward implementing BBT pro-grams is difficult to determine because researchon classical biological control sometimes resultsin significant suppression of a pest followingrelease of an imported natural enemy, althoughno funds for implementation per se wereexpended.

❚ U.S. Department of AgricultureFour U.S. Department of Agriculture (USDA)agencies conduct BBT-related work rangingfrom regulation to research, implementation, andextension. Today, their activities fall under theumbrella of policies set in place by the ClintonAdministration’s stated goals to reduce the use ofconventional pesticides and to implement inte-grated pest management (IPM) on 75 percent ofU.S. agricultural lands by the turn of the century(box 5-1).

T

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CHAPTER 5 FINDINGS

■ The federal government dominates research on biologically based technologies for pest control(BBTs). Total federal funds for research, which exceed $130 million annually, are dispersed among 11

agencies. Despite its size, this expenditure appears to be largely uncoordinated and to lack adequateprioritization.

■ Widespread agreement exists that basic research on BBTs is poorly linked to on-the-ground applica-tions. One reason is a lack of research necessary to translate findings into practical field applications,

in part because no federal research agency takes responsibility for this function.■ The U.S. Department of Agriculture’s Animal and Plant Health Inspection Service (APHIS) now has a

group of scientists developing methods for applying BBTs to control widespread pest problems. Thegroup grew out of clear needs for applied research that were not being served by the Agricultural

Research Service (ARS). Its existence engenders considerable institutional conflicts within USDA,however.

■ According to some estimates, noxious weeds that degrade western rangelands are spreading at ratesof up to 4,000 acres per day. Federal land managers consider biological control to be one of the cor-

nerstones to a cost-effective solution. However, they lack the resources to support appropriateresearch or programs, and no federal research agency has yet made a large effort in this area.

■ Attempts have been made to coordinate biological control activities within and between the federalagencies in the past. But, so far, research scientists say these efforts have been unsuccessful

because the coordinating committees and institutes have had inadequate institutional status, authority,and funding.

■ Use of BBTs generally requires a significant level of information and knowledge, and farmers oftenlack clear-cut instructions or authoritative sources of advice on how to apply them. The Cooperative

Extension Service is the principal government provider of direct, hands-on services to growers, butmost extension agents have had little if any formal exposure to biologically based approaches.

■ The Cooperative Extension Service’s role in shaping pest management practices is now secondary tothat of the more numerous private crop consultants, pest control advisors, and pesticide dealers and

applicators in most regions of the country. Like extension agents, many private advisors are not wellversed in BBTs or integrated pest management (IPM).

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TABLE 5-1: Funding for Research on BBTs

1988 1989 1990 1991 1992 1993 1994 19951996 (est.)

U.S. Department of Agriculture (USDA)

Agricultural Research Service (ARS)a 82 80 82 87 101 98 104 104 104

Cooperative State Research, Education and Extension Service (CSREES)b

Federal 6 9 9 9 9 10 12 13 14

State 24 28 31 27 28 29 29 30 30

Animal and Plant Health Inspection Service (APHIS)c

3 4 6 7 8 10 12 10 10

Forest Service 3 5 4 5 5 5 5 5 NAd

U.S. Environmental Protection Agency (EPA)

NA NA NA NA NA 1 1 1 0

U.S. Army Corps of Engineers 0.9 0.8 1.3 1.2 1.4 1.5 1.4 1.4 0

U.S. Department of Interior (DoI) NA NA NA 1 1 1 1 1 1

Total public spending 118 126 133 137 153 156 165 165 >159

Inflation-adjusted spendinge ≈109 ≈112 ≈112 ≈113 ≈124 ≈125 ≈130 ≈129 NA

a According to certain former and current ARS scientists, the ARS pest control budget has been declining since 1985. Data obtained by OTA donot confirm this assertion. According to ARS, although the pest control budget has increased modestly in recent years, its purchasing power hasdecreased; ARS consequently has been unable to fill biological control positions vacated by retirements.b Numbers cover only biological control research and do not include microbial pesticides, pheromones, sterile insects or plant immunization.c APHIS/PPQ Biological Control Operational program budget only.d NA = Not available.e The producer price index (PPI) was used to calculate inflation-adjusted research budgets. In 1982, the base year used, the PPI was 1.00; in1988 it was 0.926; in 1993, 0.802; and in 1995, it is estimated to be 0.78.

NOTE: Data have been rounded to nearest million, except for the Army Corps of Engineers. This chart presents the best numbers available. Theagencies do not usually report their budgets in categories consistent with OTA’s scope. They and OTA’s contractors exercised care in compilingthe numbers; each agency also reviewed and confirmed the budget estimates. Nevertheless, some errors of under- or overreporting may haveoccurred. An additional complexity is that it is widely acknowledged that the Current Research Information System used to track funds and full-time equivalents has technical flaws and inconsistent definitions.

SOURCES: Compiled by OTA from E.Z. Francis, Director, Toxics/Pesticides and Water Staff, Office of Research and Science Integration, U.S.Environmental Protection Agency, Washington, DC, letter to the Office of Technology Assessment, U.S. Congress, Washington, DC, June 9,1995; D.M. Gibbons, The EOP Foundation, Inc., Washington, DC, “Biologically-Based Technologies for Pest Control: Report on the Role of theUSDA in Biologically-Based Pest Control Research,” unpublished contractor report prepared for the Office of Technology Assessment, U.S. Con-gress, Washington, DC, January 1995; W. Klassen, Tropical Research and Education Center, University of Florida, Homestead, FL, letter to theOffice of Technology Assessment, U.S. Congress, Washington, DC, 1995; K. Koltes, National Biological Service, U.S. Department of the Interior,personal communication, June 1995.; D.E. Meyerdirk, Biological Control Operations, Plant Protection and Quarantine, Animal and Plant HealthInspection Service, U.S. Department of Agriculture, Riverdale, MD, fax to the Office of Technology Assessment, U.S. Congress, Washington, DC,August 3, 1995; R. Nechols and J. Obrycki, Kansas State University and Iowa State University, “OTA Preliminary Assessment of Biological Con-trol: Current Research,” unpublished report for the Office of Technology Assessment, U.S. Congress, Washington, DC, January 1994; S.J.Rockey, National Research Initiative Competitive Grants Program, Cooperative State Research, Education, and Extension Service, U.S. Depart-ment of Agriculture, Washington, DC, fax to the Office of Technology Assessment, Washington, DC, August 10, 1995.

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TABLE 5-2: Funding of BBT-Based Pest Control Programs

Agency Fiscal year 1994 dollars (millions)

Animal and Plant Health Inspection Servicea 69.7

Forest Service 11.0

States 9.4

Bureau of Land Management 0.3

a Includes all APHIS pest control programs having a major focus on BBTs.NOTE: Table does not include technology transfer functions through ARS and CSREES or classical biological control research programs in whichresearchers introduce a biological control agent.

SOURCES: D.M. Gibbons, The EOP Foundation, Inc., Washington, DC, “Report on the Role of the USDA in Biologically-Based Pest ControlResearch,” unpublished contractor report prepared for the Office of Technology Assessment, U.S. Congress, Washington, DC, January 1995;W.W. Metterhouse, Cream Ridge, NJ, “The States’ Roles in Biologically-Based Technologies for Pest Control,” unpublished contractor report pre-pared for the Office of Technology Assessment, U.S. Congress, Washington, DC, November 1994; D. Meyerdirk, Animal and Plant Health Inspec-tion Service, U.S. Department of Agriculture, Riverdale, MD, fax to the Office of Technology Assessment, U.S. Congress, Washington, DC,August 3, 1995.

BOX 5-1: USDA’s Integrated Pest Management Initiative

On September 21, 1993, at a joint congressional hearing, the U.S. Department of Agriculture (USDA),

the U.S. Environmental Protection Agency (EPA), and the Food and Drug Administration called for anational commitment to develop and implement Integrated Pest Management (IPM) on 75 percent of U.S.

crop acreage by the year 2000. The USDA announced an Integrated Pest Management Initiative inDecember of the following year. Its goals include involving farmers and practitioners in the development

of IPM programs, increasing the use of IPM systems, and developing active partnerships between thepublic and private sectors. To achieve these goals, the Administration budget for fiscal year 1996 recom-

mended a significant increase in funding for the IPM initiative’s principal programs. The budget requestsfor 1996 include $7 million for a regional competitive grants program; $9.5 million for ARS’s areawide pest

management program; and $5 million to be passed through the Cooperative State Research Educationand Extension Service to the Cooperative Extension Service and State Agricultural Experiment Stations to

meet priorities identified on a regional and local level. As of August 1995, the Congress had appropriatedno increase to the Extension Service and only $360,000 to be used for regional programs.a

The Clinton Administration’s commitment to IPM is the third attempt to create a national IPM program

since the term IPM first came into use in the 1960s. Both the Nixon and the Carter administrations fundedmultiagency research, training, and implementation programs. These programs inspired broad interest at

the state level but were unable to provide a similar sustained effort at the national level. Funding for IPMprograms was redirected after the 1980 election.

The design and direction of the Clinton Administration’s IPM Initiative is based on years of thoughtful

planning and analysis at local, regional, and national levels. In June 1992, USDA and EPA jointly spon-sored the National IPM Forum which brought together participants from all sectors involved in agricul-

ture—including 13 federal agencies—to examine constraints and obstacles to the adoption of IPM. Thefollowing year, with partial funding from EPA, several regional workshops of growers were convened in

order to follow up on the national forum. In 1994, the Experiment Station Committee on Organization andPolicy and USDA jointly funded the Second National IPM Symposium.

(continued)

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Agricultural Research ServiceAn estimated $104 million of the AgriculturalResearch Service’s (ARS) annual budget goestoward research on BBTs, supporting the effortsof around 1,166 FTEs1 (table 5-1) (114).Approximately 300 BBT-related projects wereunder way in 1993 (247). ARS represents the sin-gle largest concentration of BBT research in theUnited States. In some BBT research disciplines,the majority of U.S. scientists work for ARS; forexample, seven of the 11 U.S. specialists in bio-logical control of postharvest plant diseases2

work for ARS (161).ARS counts among its past accomplishments

complete economic control of 11 insect pests andthree weeds by classical biological control (58).

1 Full-time equivalent employees. Any given FTE in the count may represent an overall summation of part-time efforts by a number ofemployees.

2 Such diseases cause decomposition or rot on fruits, vegetables, and other commodities after they have been harvested.

The agency also played a key role in the screw-worm (Cochliomyia hominivorax) program thateradicated this pest from the United States.Ongoing BBT research includes projects such asbiological control of the rangeland weed yellowstarthistle (Centaurea solstitialis), and suppres-sion of diamondback moth (Plutella xylostella)in cabbage using a combination of pheromones,parasitic wasps, and Bacillus thuringiensis (Bt)(20,88,430).

ARS researchers working on BBTs are dis-tributed throughout the agency’s 129 laboratoriesacross the country, with biological control activi-ties occurring at 49 locations (349). The agencyalso has four laboratories abroad (Montpellier,France; Buenos Aires, Argentina; Tuxtla-Gutier-

Early in 1994, under the auspices of the Deputy Secretary of Agriculture, the planning for USDA’s IPMinitiative began. It was decided that USDA would approach IPM at state and regional levels to identify

and address the needs of growers. Essential to accomplishing this task are IPM teams composed of pro-ducers, land-grant universities, crop advisers and consultants, and private industry. In 1995, 23 teams

involving 42 states were convened to identify important research and education needs and to establishguidelines for evaluating the efficacy of USDA IPM programs. Equally important, the proposed competi-

tive grants program for funding IPM research would award grants (up to $500,000 per year for five years)to similar multidisciplinary teams to ensure that the work addresses real-world concerns of growers and

that the results feed directly into field use.

The USDA’s IPM initiative addresses a number of the criticisms raised in this chapter. It could encour-

age organization and cooperation among the federal government, states, growers, and researchers, andimprove the connection between IPM research and its implementation. Ultimately, the impact of the

USDA IPM initiative on pest management will depend on sustained commitments from USDA, the Admin-istration, and the Congress. Whether support will be forthcoming from Congress is as yet uncertain.

a This reflects wording of the agricultural appropriations bill for fiscal year 1996 from the House of Representatives; as of August1995 the Senate had not put together its agricultural appropriations bill.

SOURCES: J.R. Cate, and M.K. Hinkle, Integrated Pest Management: The Path of a Paradigm, National Audubon Society, (Alex-andria, VA: Weadon Printing, Inc., July 1994); L. Elworth, Special Assistant for Pesticide Policy, Office of the Assistant Secretaryfor Science and Education, U.S. Department of Agriculture, personal communication, May 5, 1995; B. Jacobsen, U.S. Departmentof Agriculture, Washington, D.C., fax to OTA, August 17, 1995; U.S. Department of Agriculture, Cooperative State Research, Edu-cation and Extension Service, “Request for Proposal, National Integrated Pest Management Implementation Program, Fiscal Year1995,” special projects guidelines, unpublished white paper, 1995; U.S. Department of Agriculture, Office of Communications,“USDA’s Integrated Pest Management,” (IPM Initiative, Release No. 0942.94, December 14, 1994).

BOX 5-1: USDA’s Integrated Pest Management Initiative (Cont’d.)

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rez, Mexico; and Panama) that conduct foreignexploration for classical biological controlagents, as well as worksites in Australia, Italy,and Greece (320). No other federal or stateagency possesses this capability for foreignexploration; although some state agencies, uni-versities, and private organizations conduct for-eign exploration, and other federal agencies (theAnimal and Plant Health Inspection Service, theForest Service, and the U.S. Fish and WildlifeService) sometimes contract with internationalorganizations to help identify potential biologicalcontrol agents. Nevertheless, ARS’s effortunderlies numerous high-priority U.S. efforts inclassical biological control (188,246,416).

ARS’s pest research focuses on certain cate-gories of pests more than others. Projectsaddressing insect pests account for approxi-mately 75 percent of its BBT research (247). Theremaining 25 percent is divided among plantpathogens (11 percent), nematodes (2 percent),and weeds (12 percent) (247).

Federal land managers believe that rangelandweeds are important pests and that BBTs couldplay an integral role in controlling them (388).ARS’s approximately $6 million weed-relatedwork takes place primarily at the RangelandWeeds Laboratory at Bozeman, Montana (280).The laboratory is relatively small, with a staff offour ARS scientists. The Forest Service has alsoassigned a scientist to the laboratory and pro-vides $300,000 annually to fund the researcher’swork. The Clinton Administration’s budget pro-posal for fiscal year 1996 would end funding forARS’s other long-standing California-based pro-gram for biological control of weeds, although itspast successes in weed control have been highlyvalued by state officials and others (26). Despitethe relatively small allocation of resources by theagency, federal land managers give ARS scien-tists high marks for their collaborative efforts toaddress rangeland weeds. For example, ARSrecently compiled a comprehensive summary offindings on weed natural enemies for use by fed-eral, state, county and other rangeland managers(348).

The major criticisms of ARS are that, despitethe agency’s accomplishments, it has difficultyresponding in a timely fashion to externally iden-tified research goals and priorities, and too muchof its BBT research does not find its way intoapplications on the ground. A number of factorsmay contribute to these problems. In general,ARS does not seem to have found a satisfactoryway to set research goals and at the same timeenable creativity and productivity among its sci-entific staff in accomplishing these goals. A sur-prisingly large number of former and currentARS staff reported their concerns about theagency’s internal management to OTA duringthe course of this assessment.

The process by which ARS allocates funds toresearch, on paper, seems to provide a clearmechanism for focusing efforts on nationalresearch goals through involvement of theNational Program Staff (figure 5-1). The scientistin the role of a National Program Leader is sup-posed to provide national leadership for a spe-cific topic area. At least three National ProgramLeaders deal with BBTs. However, in practice,because the National Program Leaders lack fund-ing authority, their influence on the overallresearch agenda—based on consultation andconsensus building among ARS scientistslocated in laboratories across the country—islargely voluntary and sometimes ineffectual.Congress has with some regularity set de factoresearch goals by targeting appropriations forwork on certain key pests, and ARS solicitsrelated research proposals from staff scientists.According to agency critics, the quality ofresearch can suffer when such political pressuresrun high (200).

Even when clearly identified goals emerge,the agency’s structure imparts an inflexibilitythat can make it difficult to reallocate resourcesand staff to newly identified priorities. Existingresources are usually tied up in ongoing projects,reflecting the long periods of time required forcertain types of research. However, this alsoleaves little funding for new initiatives. In addi-tion, ARS managers say scrutiny by members ofCongress can strongly deter attempts to move

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Agricultural Research Service

I I

Peerreview

I

I

State Agricultural Experiment Stations(CSREES)

Headquarters(Washington)

review/approval

ESCOP Stationcoordination director

Station

consensus buildingdirector

approval

TPeer

review

START

SOURCE: Office of Technology Assessment, 1995,

NOTE: Dashed line represents influences of the National Program Leaders (NPL) or the Experiment Station Committee on Organization and Pol-

icy (ESCOP).

projects from one congressional district toanother even when warranted by changing pestproblems (349). Experience with the silverleafwhitefly, Bemisia argentifolii, (formerly knownas the sweetpotato whitefly strain B, Bemisiatabaci) demonstrates ARS’s limitations inresponding rapidly to emerging pests (box 5-2)(200). The agency was unable to mobilize a sig-nificant research effort until after the five-yearUSDA program was put into effect. By that time,the pest had risen to the top of the politicalagenda and funds were directed to the Animaland Plant Health Inspection Service (APHIS) forits control.

Perhaps in part because of such delays, ARS’sresearch does not always match the needs ofoperations agencies involved in pest manage-ment. For many years APHIS, the agency with

principal responsibility for control of agriculturalpests, annually submitted a prioritized list ofresearch needs to ARS (364). APHIS representa-tives say the agency was unable to identify tangi-ble results that supported their operationalresponsibilities (364) and consequently in 1992moved to less formal methods for communicat-ing their needs (428). According to ARS, how-ever, virtually all of APHIS’s ongoing biologicalcontrol programs are based on research accom-plished by ARS; the role of APHIS’s methodsdevelopment staff (discussed later) has been toscale-up the findings from ARS research (320).The differing views suggest that, although ARSresearch does support APHIS operations, itrequires significant adaptation to be put intopractical use. The differing views also seem

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BOX 5-2: Case Studies of USDA Pest Control ProgramsInvolving Biologically Based Technologies

Eradication of the screwworm

The screwworm (Cochliomyia hominovorax, the larval stage of the screwworm fly) is a parasite thatconsumes the live flesh of cattle, hogs, horses, mules, sheep, goats, dogs, other domestic and wild ani-

mals, and humans. During the first half of the century, this pest caused significant damage in the south-ern United States. For example, between 1932 and 1934, 1.3 million livestock animals were infested by

the parasite, and over 200,000 animals died in the Gulf states.

In 1951 USDA began a program to eradicate the screwworm from the United States by releasing ster-

ile male screwworm flies into wild populations. Poor management of the production and distribution of theflies and misunderstandings of the pest’s behavior and ecology led to setbacks in the Southwest between

1972 and 1976. Program scientists identified the main causes of the problems, and, by 1982, the screw-worm became the only pest to be eliminated from the United States.

The screwworm program began prior to the separation of APHIS and Agricultural Research Service

into two distinct agencies. After the separation, these two agencies worked together on the program untilthe mid-1980s. APHIS continues the program today in Mexico and Central America.

The scientists involved in the program attribute its success to several factors, including USDA’s long-

term commitment and sustained funding. Staff for the eradication program devote 100 percent of theirtime to it; in contrast, other USDA scientists work on several projects at once. Other contributing factors

include regulations to control the movement of infested cattle, and cooperation among veterinarians,farmers, and federal officials. The eradication program in Mexico has been less successful partly

because of the continued movement of contaminated cattle.

The boll weevil eradication program

Since 1892 the boll weevil (Anthonomus grandis) has caused considerable damage to the U.S. cotton

industry. Aggregate losses amounted to $12 billion as of 1990. Losses per year in the mid-1970s wereestimated at $200 million to $300 million. In the 1960s ARS began a program to eradicate the boll weevil

from the southeastern United States. The main objectives were to reduce economic damage from thepest, to reduce the use of pesticides, and to conserve the natural enemies of the other pests in cotton

fields such as the beet armyworm (Spodoptera exigua), fall armyworm (S. frugiperda), and bollworm, alsocalled the corn earworm and the tomato fruitworm (Helicoverpa zea). To date, the boll weevil eradication

program has succeeded in eight of the cotton belt states, while four others are engaged in on-going pro-grams. Farmers have gained $12 for every dollar they have spent on this program. Because of

decreased pesticide sprayings against the boll weevil, the beet armyworm and fall armyworm are nowcontrolled by their natural enemies in many cotton fields.

Success of this program has been attributed to the strong coordination among federal agencies, state

governments, and farmers. APHIS coordinates the overall program with the Boll Weevil Eradication Foun-dation, organized by the farmers who provide a majority of the funding. Farmers usually supply over 70

percent of the program funds, while the remainder comes from USDA (mainly APHIS) and the state gov-ernments. Although areawide spraying of pesticides is the main control method, a pheromone trap for

monitoring boll weevil abundance, developed by ARS, is an essential component of the program. Afterthe areawide sprayings, traps allow fieldworkers to detect and take action against each new infestation

before the pest becomes abundant and spreads to uninfested fields.

(continued)

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Chapter 5 From Research to Implementation | 117

Russian wheat aphid

The Russian wheat aphid (Diuraphis noxia) first appeared in the United States in 1986 and has sincespread to 15 states and caused more than $850 million in losses to wheat farmers. In 1988, scientists

from APHIS, the Agricultural Research Service, and CSREES began research to identify classical biologi-cal control agents for the Russian wheat aphid.

APHIS has received a majority of the congressional line-item funds for the control of this pest—between $1 million and $2.5 million annually from 1990 to 1995. The agency’s biological control program

has not yet succeeded in establishing any natural enemies that provide adequate control. Scientists criti-cize APHIS for putting too much emphasis on the introduction of potential biological control agents while

neglecting to carry out effective followup studies tracking the agents’ impacts. Little is known about theeffects, good or bad, of the introduced species on the Russian wheat aphid, on other introduced natural

enemies, or on native species and ecosystems. Of the 24 species and over 100 geographic strainsreleased, only four of the imported parasites are suspected of having become established in the wheat-

fields, and their effectiveness against the Russian wheat aphid remains unknown. Field workers and sci-entists are unable to correctly identify the released parasites because of their close resemblance to

native strains and to other parasites released by ARS for control of different aphid pests. Some aphidpredators (which are mainly lady beetles) released by APHIS prior to the Russian wheat aphid program

have also become established, although their effectiveness against the pest is uncertain.

Scientists involved in the program feel it is too early to judge its success because establishing aneffective biological control agent can take years. Others argue, however, that the program has been

rushed because of APHIS’s responsibility to suppress pest outbreaks. The result has been the release ofnumerous natural enemies without correct identification of their taxonomy or adequate knowledge of their

ecological effects. Biological control programs lacking such information are less likely to succeed. Forthis reason, biological control is not often the best route for quick suppression of a pest, unless adequate

knowledge is available at the project’s inception about the ecology of both the pest and its natural ene-mies.

The silverleaf whitefly

The silverleaf whitefly (Bemisia argentifolii)—initially identified as strain B of the sweet potato whitefly(Bemisia tabaci)—first appeared in Florida in 1986. It attacks at least 600 different crops, including

melon, cotton, tomato, lettuce, and many ornamental plants. The spread of the silverleaf whitefly acrossthe country caused extensive crop losses estimated at $200 million to $500 million between 1991 and

1992. The Imperial Valley of California has been one of the hardest hit areas; from 1991 through 1994, anestimated 9,000 local jobs disappeared and crop losses exceeded $300 million due to the pest.

The initial response of scientists and federal agencies to the silverleaf whitefly was uncoordinated and

lacking in focus. Scientists who began studying the problem were working in isolation, and thus their workwas unlikely to yield rapid solutions. Despite warnings in the late 1980s by its own scientists, ARS began

to mobilize a significant response to the pest only when damage skyrocketed during the 1991 outbreak inthe Southwest. And according to numerous critics, APHIS and ARS had difficulty cooperating during

early phases of the outbreak. USDA officials attribute the early inaction to the lack of an official mecha-nism for USDA agencies to jointly address new pest problems.

(continued)

BOX 5-2: Case Studies of USDA Pest Control ProgramsInvolving Biologically Based Technologies (Cont’d.)

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characteristic of the lack of good communicationand cooperation between ARS and APHIS.According to outside observers, even ARSresearch results that might be relevant toAPHIS’s programs do not consistently filterthrough to APHIS because of poor communica-tion between the agencies (114,176).

The working environment for individual sci-entists within the agency may also affect the easewith which ARS’s research on BBTs moves intopractical applications. Agency scientists com-plain that the funding environment is highlycompetitive, and that funds get siphoned off atseveral levels, leaving only a minimum amount

Actions by grower organizations and commodity groups played a significant role in improving thefocus of efforts to control the silverleaf whitefly. These groups lobbied for congressional action, resulting

in direct appropriations in fiscal year 1993 of $2.6 million to APHIS for the development of a biologicalcontrol program. The Office of the Secretary of Agriculture stepped in to provide guidance in develop-

ment of a cooperative USDA program; in 1992 the five-year action plan was put in place to coordinate theefforts of ARS, APHIS, CSREES. The grower and commodity groups also supplied direct funding to local

extension scientists, which supported the essential research for developing local and regional controlmethods.

To date, the most effective measures for controlling the silverleaf whitefly are cultural practices, chem-

ical insecticides, and a microbial pesticide based on the fungus Beauvaria bassiana. APHIS’s biologicalcontrol program has not yet yielded a successful natural enemy. As in the case of the Russian wheat

aphid, the agency has been criticized by outside scientists for releasing multiple biological control agentswith too little forethought or post-release monitoring.

SOURCES: S.L. Birdsall and D. Ritter, Imperial Valley Agricultural Commissioner and Whitefly Program Coordinator, respectively,unpublished data on the economic impact of the silverleaf whitefly in Imperial Valley, Imperial Valley, CA, 1994; H. Browning,State Agricultural Experiment Station, University of Florida, Gainsville, FL, personal communcation, August, 1995; W. Dickerson,Plant Pest Administrator, North Carolina Department of Agriculture, Raleigh, NC, personal communication, July, 1995, and August1995; T. Engle, Budget and Accounting Office, Animal and Plant Health Inspection Service, U.S. Department of Agriculture, River-dale, MD, fax to the Office of Technology Assessment, U.S. Congress, Washington, DC, August 21, 1995; M.J.R. Hall and W.N.Beesley, “The New World screwworm fly in North Africa,” Pesticide Outlook 1(2):34-37, 1990; P. Karieva, Department of Zoology,Univeristy of Washington, Seattle, WA, fax to the Office of Technology Assessment, U.S. Congress, Washington, DC, August,1995; E.S. Krafsur, Department of Entomology, Iowa State University, Ames, IA, personal communication, July, 1995; W. Lambert,extension entomologist, Univeristy of Georgia, personal communication, August, 1995; N. Leppla, Assisstant Director, NationalBiological Control Institute, Animal and Plant Health Inspection Service, U.S. Department of Agriculture, Riverdale, MD, personalcommunication, August, 1995; R.L. Metcalf and R.A. Metcalf, Destructive and Useful Insects: Their Habits and Control 5th Ed.(New York, NY: Mcgraw-Hill Inc., 1993); S.K. Narang, National Program Staff, Agricultural Research Service, U.S. Department ofAgriculture, Beltsville, MD, fax to Offfice of Technology Assessment, U.S. Congress, Washington, DC, August 17, 1995; J.R.Nechols, Department of Entomology, Kansas State Univerisity, Manhattan,KS, personal communication, July 24, 1995, August 21,1995; D. Prokrym, Project Leader, Russian Wheat Aphid Biological Control Project, Animal and Plant Health Inspection Service,U.S. Department of Agriculture, Niles, MI, personal communication, August 10, 1995, letter to the Office of Technology Assess-ment, U.S. Congress, Washington, DC, August 11, 1995; D. Stanley, “Whitefly Causes Bleak Times for Growers,” AgriculturalResearch 16(2), January, 1991; N. Toscano, Department of Entomology, Univeristy of California-Riverside, Riverside, CA, per-sonal communication, August, 1995; U.S. Department of Agriculture, Animal and Plant Health Inspection Service, “Biological Con-trol of the Russian Wheat Aphid,” APHIS Pub. No. 1507 (Washington DC: December 1993); U.S. Department of Agriculture,Animal, and Plant Health Inspection Service, Plant Protection and Quarantine, National Biological Control Laboratory, RussianWheat Aphid Biological Control Project—FY 1993 Project Report, prepared by D.R. Prokrym, J.R. Gould, D.J. Nelson, L.A. Woodand C.J. Copeland (Niles, MI: 1993); U.S. Department of Agriculture, Economic Research Service, Economic Returns to Boll Wee-vil Eradication, prepared by G.A. Carlson, G. Sappie and M. Hammig, AER Pub. No. 621 (Washington, DC: September 1989); R.Van Driesche, et al. Department of Entomology, Univeristy of Massachusetts, Amherst, MA, “Report on Biological Control of Inver-tebrate Pests of Forestry and Agriculture,” unpublished contractor report prepared for the Office of Technology Assessment, U.S.Congress, Washington, DC, December 1994.

BOX 5-2: Case Studies of USDA Pest Control ProgramsInvolving Biologically Based Technologies (Cont’d.)

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for actually conducting the research. Some low-profile areas central to the development of BBTs,such as taxonomy and systematics, receive rela-tively little support (58). According to some ARSscientists, the necessary work to take research onBBTs “out of the laboratory and into the field” isdiscouraged. Instead, performance is judged bythe number of scholarly publications—a criterionusually applied to academic scientists whosework is supposedly less mission oriented.

One mechanism for converting researchresults into practical applications is the Coopera-tive Research and Development Agreements(CRADAs) through which outside institutionshelp to fund federal research and obtain licensingrights to research discoveries in return. ARS hassupported numerous collaborative researchprojects with private industry (320). As of July1994, ARS had a total of 16 ongoing agreementsrelated to BBTs. However, only five of theseinvolved private sector companies or organiza-tions; the rest were agreements with other federalagencies, states, foreign governments, or univer-sities (300). ARS recently began to developanother new program for transferring technolo-gies to the private sector that might provide addi-tional opportunities for companies to help fundARS research; the program is expected to start infiscal year 1996 (417A) (see options in chapter 6for additional discussion of cooperative agree-ments with the private sector).

ARS scientists working on classical biologicalcontrol express specific dissatisfaction with theorganizational structure of the agency and how itaffects their ability to do timely work. They pointto the 1972 restructuring of the agency as a majorblow because it destroyed the previous tightcoordination of related research within theagency (58). ARS had a National ProgramLeader for Biological Control until 1992 whenthe program was changed to Pest Management.Coincident with a switch in senior management,

the emphasis changed back to Biological Controlin 1995 (349). Whether this action will help pro-vide the focus and coordination ARS scientistsdesire in the area of biological control is uncer-tain.

Overall, ARS as a research institution hasgreat capabilities in the area of BBTs. Improvingthe flow of research findings into the field tosolve real-world pest problems poses a numberof challenges, however.

Animal and Plant Health Inspection ServiceThe Animal and Plant Health Inspection Service(APHIS) has significant responsibilities for pro-tecting American agriculture from pests underthe Plant Pest Act, the Federal Noxious WeedAct, and the Plant Quarantine Act.3 Its functionsrelated to the regulation of natural enemies arediscussed in further detail in chapter 4. This sec-tion focuses on APHIS’s pest control responsi-bilities.

APHIS’s pest control programs incorporate anumber of BBTs (table 5-3). The agency hasplaced special emphasis on biological control. In1992 the APHIS Administrator issued an agen-cywide policy directive (the APHIS BiologicalControl Philosophy) stating:

APHIS believes that modern biological con-trol, appropriately applied and monitored, is anenvironmentally safe and desirable form oflong-term management of pest species. APHISbelieves that biological control is preferablewhen applicable; however, we also recognizethat biological control has limited application toemergency eradication programs. Where possi-ble, biological control should replace chemicalcontrol as the base strategy for integrated pestmanagement (222).

In 1994, the North American Plant ProtectionOrganization4 adopted a similar philosophybased on APHIS’s model (197). University andstate scientists outside the federal government,

3 Federal Plant Pest Act (1957), as amended (7 U.S.C. 147a et seq.), the Federal Noxious Weed Act (7 U.S.C. 2801 et seq. (1974)) and thePlant Quarantine Act (7 U.S.C. 151 et seq. (1967)).

4 The North American Plant Protection Organization is part of the International Plant Protection Group that is comprised of representa-tives from Canada, Mexico, and the United States.

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TABLE 5-3: Technologies Used in Pest Management Programs of the Animal and Plant Health Inspection Service (USDA)

Pest Biological controlSex pheromone

trapSterile insect

technique Other

Insects

Apple ermine moth (Yponomeuta malinella) X P

Boll weevil (Anthonomus grandis) X X P, C, F

Brown citrus aphid (Toxoptera citricida) X

Cereal leaf beetle (Oulema melanopus) X

Cherry ermine moth X P

Euonymus scale (Unapis euonymi) X

Fruit fly detection X P, F, M

Grasshopper/MC X, MD P

Gypsy moth (Lymantria dispar) X, MD X MD P

Imported fire ant (Solenopsis invicta, S. richteri) MD P

Japanese beetle (Popillia japonica) X X P

Medfly (Ceratitis capitata) MD X X P, F, M, C, E

Mexfly (Anastrepha ludens) MD X P, F, C, E

Pine shoot beetle (Tomicus piniperda) X P, MT, C, E

Pink bollworm (Pectinophora gossypiella) X X X P,C, E

Russian wheat aphid (Diuraphis noxia) X

Sweet potato whitefly (Bemisia tabaci) X

Weeds

Common crupina (Crupina vulgaris) X

Diffuse and spotted knapweed (Centaurea diffusa, C. maculosa)

X

Leafy spurge (Euphorbia esula) X C

Purple loosestrife (Lythrum salicaria) X

Catclaw mimosa (Mimosa pigra) P

Onionweed ( Asphodelus fistulosus) P

Goatsrue (Galega officinalis) P

Hydrilla (Hydrilla verticillata) X P

Little bell morning glory (Ipomoea triloba) P

Liverseed grass (Urochloa panicoides) P

Mediterranean saltwort (Salsola vermiculata) P

Branched broomrape (Orbanche ramosa) P

Small broomrape (Orbance minor) P

(continued)

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Chapter 5 From Research to Implementation | 121

however, are somewhat skeptical about theextent to which APHIS adheres to the policy(338A).

Although APHIS has identified 10 criteria forselecting target pests for biological control, theagency says that advice from the National PlantBoard5 and political considerations often emergeas the most significant factors (365). APHIS cur-rently funds 14 pest control programs based onbiological control at a total annual cost ofapproximately $11 million (230). Half of thismoney is committed in designated budget linesto only two pests. The agency has long com-plained that such a precise designation of fundsfor specific pests decreases its ability to respondto newly emerging pest threats. However, thedesignation also ensures that the money goes tothe specific pest problem and is not diffusedamong several programs. Biological control pro-grams often affect several states and, conse-quently, involve significant allocations of funds.

5 The National Plant Board is composed of federal agriculture officials and individuals from state departments of agriculture.

The APHIS program for leafy spurge (Euphorbiaesula), for example, covers 17 western states andcost $1.8 million in fiscal year 1994 (356).

One measure of the agency’s commitment tobiological control was the creation of theNational Biological Control Institute in 1990 inresponse to a perceived need to increase theprominence of and coordinate biological controlwithin APHIS, between APHIS and the otherUSDA agencies, and between APHIS and orga-nizations outside the government. The institute’smission is “to promote, facilitate and provideleadership for biological control” (363).

APHIS created the National Biological Con-trol Institute the same year the USDA establishedthe Interagency Biological Control CoordinatingCommittee (“IBC3”) by a memorandum signedjointly by the administrators from ARS, theCooperative State Research Service,6 andAPHIS. Two other USDA agencies, the ForestService and the Extension Service, also partici-

6 The Cooperative State Research Service (CSRS) has since been merged with the Extension Service to become the Cooperative StateResearch, Education, and Extension Service (CSREES). CSREES is discussed later in this chapter.

Witchweed (Striga spp.) CS

Plant pathogens

Black stem rust (Puccinia graminis) C, RV

Chrysanthemum white rust (Puccinia horiana) P, RV

Golden nematode (Globodera rostochiensis) C, RV

TABLE KEY:X = UsedC = Cultural controlCS = Chemical stimulantE = Environmental (hot or cold air treatment)F = Food bait trapMD = Methods under developmentMT = Mechanical Trap (traps of a particular shape , size, or color)P = PesticideRV = Resistant varietiesSterile Insect = Use of sterile insects

SOURCE: U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine, Biological Control Oper-ations, unpublished 1994 data provided by D. E. Meyerdirk, Senior Staff Officer, April 1995.

TABLE 5-3: Technologies Used in Pest Management Programs of the Animal and Plant Health Inspection Service (USDA) (Cont’d.)

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pated. The committee’s purpose—“to provideleadership in biological control within USDAand in proposing uniform departmental policiesin such matters” (119)—was similar to that of theNational Biological Control Institute. Unlike theinstitute, however, the committee never had anydirect funding. In 1993, the committee attemptedto make biological control a top USDA priorityby proposing a National Biological Control Pro-gram to enhance biological control research, edu-cation, and implementation efforts in the federalgovernment. That program called for an increaseof $53 million over three years. Both the Cooper-ative State Research Service and APHISreceived small allocations of funds in 1994 asso-ciated with the proposed program, but the pro-posal was never fully acted upon (75,324). As of1995, the Interagency Biological Control Coordi-nating Committee had lapsed into inactivity.

Reviews of APHIS’s National BiologicalControl Institute’s impacts are mixed. The insti-tute is effective at outreach beyond the beltwayand is highly respected by scientists in state gov-ernment, universities, and other institutions.Over the past four years, the institute hasawarded approximately $1.5 million in grants forimplementation projects, educational and infor-mational materials, postdoctoral fellowships,meetings and workshops, publications and thedevelopment of databases (363). However, theinstitute’s highly regarded staff and expertise arenot always paid attention to within APHIS. Forexample, efforts by the National Biological Con-trol Institute to involve stakeholders in the devel-opment of biological control regulations werenot incorporated into the broader proposed rulethat APHIS issued for nonindigenous species(see chapter 4). That rule was later withdrawnbecause of negative public comment. APHIS isnow starting a new rulemaking process in whichthe agency again will seek out extensive publicinput (353). Moreover, the institute has not beenincorporated into the working group representing

various agencies in the USDA IPM Initiative.This oversight is unfortunate because it perpetu-ates the historical separation of biological controland IPM pest control disciplines (see chapters 2and 3 for discussions of the relationship betweenbiological control and IPM).

To support its implementation programs,APHIS has a methods development staff whichconducts applied research on how to get BBTmethods into the field to solve widespread pestproblems. About $5 million is expended annuallyon biological control research, and $10 millionoverall on all BBTs (230).7 APHIS created theMethods Development because ARS and otherresearch agencies were not adequately address-ing APHIS’s pest control development needs,especially the scale-up necessary to apply meth-ods more broadly. The existence of the methodsdevelopment staff within APHIS is a source ofsome tension with the USDA research agencies,however. In 1991, when the Secretary of Agri-culture initiated the silverleaf whitefly program,critics argued that APHIS should not havereceived funding for implementing a control pro-gram until more basic research by other agenciesand scientists had demonstrated that technologieswere available to control the pest (78). The criti-cism perhaps reflects an inherent overlapbetween research and implementation programsin classical biological control. The desired end-point of both is the establishment of a naturalenemy that provides widespread, lasting, andeffective suppression of a pest; in national pestcontrol programs the respective roles of researchby ARS and implementation by APHIS inachieving this goal have not yet been well delin-eated.

A related concern is whether APHIS can oper-ate objectively in regulating its own biologicalcontrol programs (82). Critics point to what theyclaim are fast-paced and sloppy attempts to putbiological control in place when a new pest risesto the top of the political agenda. Because of a

7 In addition to Methods Development, APHIS’s Animal Damage Control Division spends about $1.3 million annually developing BBTsfor vertebrates, specifically immunocontraceptives and genetically engineered vaccines for coyotes (225)

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Chapter 5 From Research to Implementation 123

Federal programs based on the release of sterile insects haveeliminated the screwworm (Cochliomyia hominivorax) from theUnited States.

Agricultural Research Service, USDA

lack of communication, these efforts sometimesinterfere with those of scientists in ARS or theState Agricultural Experiment Stations, erodingtheir relationships with APHIS (246). Experiencewith the Russian wheat aphid (Diuraphis noxia)and silverleaf whitefly tend to support this view(box 5-2). Regulatory, research, and implementa-tion functions related to biological control allcoexist in the same organizational unit of APHIScalled Plant Protection and Quarantine. This situ-ation creates significant potential for internalpressuring of regulators to expedite permitting ofnew biological control introductions, especiallywhen there is great political urgency to find solu-tions to existing pest problems.

APHIS has statutory authority to conduct pestcontrol programs and to regulate biological con-trol introductions. The agency also has a legiti-mate role in developing methods to apply BBTsin the field, because these needs are not currentlymet by any other agency. Better insulation ofeach of these functions from one another, how-ever, would perhaps ensure the best performanceof all three. The current trend within APHIS mayrun in the reverse direction, however. Theagency recently downgraded its operational bio-

logical control program (including the laborato-ries) and placed it under authority of the methodsdevelopment staff. State agriculture departmentshoping to increase the level of coordination ofbiological control activities worry that APHIS’saction will result in a loss of identity, effective-ness, and funds for biological control operations(229).

Forest ServiceThe Forest Service manages the 191.5 millionacre National Forest System (roughly 8 percentof the U.S. land area and 29 percent of all feder-ally administered lands). The system encom-passes 156 national forests, 19 nationalgrasslands, and 98 other units (334). In addition,under the Cooperative Forestry Assistance Act,the Forest Service controls insect pests and dis-eases on other forested areas in the country (pub-lic and private, some through various cost-share

8 To fulfill these responsibilities,arrangements).the agency has units for pest managementresearch, Forest Insect and Disease Research(FIDR), and for pest suppression, Forest HealthProtection (FHP).

FIDR received $24 million in fiscal year 1994for pest management research, of which approxi-mately $4.5 million was used to fund work onBBTs (114,324). The latter amount was dividedbetween biological control (approximately $3.1million) and behavioral chemicals ($1.4 million)(114). Among funded projects in fiscal year 1995are two new biological control studies for range-land weeds ($300,000) and hemlock woody adel-gid (Adelges tsugae) ($150,000), with foreignexploration for natural enemies being conductedout of the ARS laboratory in Europe (320,324).The Forest Service established a quarantine facil-ity in Ansonia, Connecticut, in 1992 to facilitateand accelerate the agency’s research and devel-opment of biological control (58). Research onBBTs is likely to increase as a result of theagency’s 1993 strategic plan, “Healthy Forestsfor America’s Future,” which emphasizes eco-

8 Cooperative Forestry Assistance Act of 1978, as amended (7 U.S.C A. 2651-2654; 16 U.S.C.A. 564 et seq.”)

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National programs to suppress the gypsy moth (Lymantria dis-par) are based largely on Bt and the gypsy moth NPV virus.

system management and calls for increases in theresearch, development, and use of biologicalcontrol, microbial pesticides, and pheromones(381A).

FHP conducts a wide array of pest controlprograms. Those programs targeting insect pestsrely to a significant extent on BBTs. In fiscalyear 1994, BBTs were used for over half of thealmost 14,000 acres of National Forests treatedfor insect pests (383). The diverse methodsinvolved include pheromones and microbial pes-ticides based on Bt, fungi, viruses, and nema-todes (383). The largest pest management efforttargets the European gypsy moth (Lymantria dis-par), relying primarily on Bt, gypsy moth NPVvirus, and pheromones to monitor distribution. In1995 the Forest Service plans to use Bt to controlthe gypsy moth on 505,603 acres and the NPVvirus on 2,263 acres of federal and cooperativelands. Total cost of the gypsy moth program infiscal year 1994 was $11 million, of which $8.3million went to Bt applications.

Conventional pesticides remain FHP’s methodof choice for other pest categories, however. Infiscal year 1994 more than 54,000 acres ofNational Forests were treated for plant pathogenswith chemical fungicides and fumigants, andalmost 38,000 acres were treated for weeds withchemical herbicides (383). Use of natural ene-mies against weeds that same year occurred on6,400 acres (383).

According to Forest Service insiders, theresearch unit, FIDR, has not always been able toprovide the solutions required by the agency’soperations unit, FHP. Part of the problem is thatthe research timetable does not always match theneeded expediency for pest control because sometechniques may require significant, and time-consuming, basic research before they can be putinto practice (a problem similar to that experi-enced by ARS). Moreover, although FHP andFIDR conduct joint programs, the researchers atFIDR rarely communicate with the land manag-ers, leading to the criticism that FIDR is not con-nected to the field. Like APHIS, FHP has begunconducting research on field applicationsbecause FIDR cannot fulfill all of its needs.Researchers worry, however, that the quality ofbiological control work will decline as the num-ber of people involved increases. Some of theseproblems may dissipate somewhat as the ForestService moves increasingly toward trying tomanage forests to prevent pest problems (i.e.,maintaining “forest health”) rather than reactingto pest outbreaks.

The Forest Service has only recently begun toaddress problems with rangeland weeds on fed-eral lands. One Forest Service scientist has beenassigned to the ARS Biological Control ofWeeds Laboratory in Bozeman, Montana (280).The Forest Service is also a member of the Fed-eral Interagency Committee for the Managementof Noxious and Exotic Weeds that was estab-lished in 1994 to coordinate federal effortsrelated to the identification and management ofweed problems.

Cooperative State Research,Education, and Extension ServiceThe Department of Agriculture ReorganizationAct of 1994 combined the mission and functionsof the Cooperative State Research Service withthose of the Extension Service (the Federal part-ner in the Cooperative Extension Service) to cre-ate the Cooperative State Research, Education,and Extension Service (CSREES) (98). The goalof reorganization was to pull together theresearch and higher education funding of the

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Cooperative State Research Service and the tech-nology transfer and education program responsi-bilities of the Extension Service in order toimprove the movement of research findings toapplication and use via education. The completeintegration of the two former agencies has notyet been accomplished; most notably, their bud-gets remain separate. This section describes theresearch-related functions of CSREES. The roleof CSREES in education and technology transferwill be discussed later in the chapter in the sec-tion dealing with educating and influencing usersof pest control.

CSREES administers federal research fundsthrough the the National Research Initiative(NRI) and through formula funds and specialgrants directed to land grant universities by wayof the State Agricultural Experiment Stations.The National Research Initiative is a competitivegrants program that funds more fundamentalresearch. These characteristics separate it fromother sources of agricultural research funding.The program was established in 1991 followingrelease of the 1989 National Research Councilreport “Investigating Research: A Proposal toStrengthen the Agricultural, Food, and Environ-ment System.” The study concluded that funda-mental research in agriculture is underfunded.Although 70 percent of funds go to the land grantuniversities, grants from the National ResearchInitiative also support research of academic sci-entists not associated with land grant universitiesand of ARS scientists (247,292). Grants totalingapproximately $13 million were awarded to bio-logical control and IPM research in fiscal year1994 (291). Of the 31 existing National ResearchInitiative programs, BBT research may befunded by any of seven programs (depending onthe focus), including Entomology, Nematology,Weed Science, and Plant Pathology (292,371). Aseparate funding program specifically for biolog-ical control began in 1994 (371). The moneycame from a congressional line item for regionalIPM that was eliminated in the 1996 House of

Representatives budget proposal; its ultimate fatewas uncertain as of August 1995 (291).

Within the National Research Initiative, BBTresearch is identified as mission oriented,although funded projects range from more basicto more applied. The application for funding asksfor information about how results will relate todevelopment of IPM programs (371). Accordingto Sally Rockey, division director of the NationalResearch Initiative, this applicability to pest con-trol programs does influence research fundingdecisions. CSREES can increase scientists’ will-ingness to consider applications of their workthrough specific calls for more mission-orientedresearch in announcements of funding opportuni-ties (292). Funding recommendations are madeby a panel of researchers who rank submittedproposals following external review and thenmake recommendations to the Chief Scientist ofthe National Research Initiative. A ScientificAdvisory Committee provides additional adviceon programmatic issues (292).

The Land Grant Universities and the StateAgricultural Experiment Stations are researchinstitutions established within the states by theLand Grant Act (also known as the Morrill Act)and the Hatch Act,9 respectively. The LandGrant University System was designed to pro-vide higher education, especially to the childrenof farmers and industrial workers, and to applyresearch knowledge to the solution of society’sproblems through outreach and extension pro-grams (337). The Hatch Act created a researchpartnership between the federal government andthe states by providing funding for the StateAgricultural Experiment Stations. These stationsare the sites of much of the nation’s agriculturalresearch. Formula funds are provided under theact and then matched by the states. These funds,as well as other competitive grants, are funneledthrough CSREES. For fiscal year 1995, CSREESdirected $13 million in federal funds towardsbiological control research through the NationalResearch Initiative and the State Agricultural

9 Hatch Act of 1887, as amended (7 U.S.C. 361a-361i).

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Experiment Stations. States provided an addi-tional $30 million in matching funds (114,292).

In comparison with the role of the directors ofthe State Agricultural Experiment Stations,CSREES has a minor role in allocating formulafunds to specific research projects (figure 5-1).Scientists submit research proposals to the sta-tion directors for internal review; the directorshave a good deal of discretion in their fundingdecisions (265). Proposals that are endorsed aresubmitted to the CSREES headquarters in Wash-ington, D.C., for final approval. Each stationdirector then designates funds from that agricul-tural station’s budget to approved projects (265).

Directors of the State Agricultural ExperimentStations make their decisions within the contextof broad strategic plans (90). Since 1986, theseplans—national guidelines setting the vision andmission for the State Agricultural ExperimentStations—have been set in place every four yearsand periodically updated by the Experiment Sta-tion Committee on Organization and Policy.10

The broad nature of these plans and the diffusionof funding authority regionally among stationdirectors, however, means that the State Agricul-tural Experiment Station System, like ARS, lackseffective mechanisms to address national goals(316).

An additional aspect of the system of stateagricultural experiment stations and land grantuniversities is how it reflects state trends. Seniorfaculty at some of the nation’s universities com-plain that as the state priorities shift (from agri-cultural to urban), allocations of faculty slots andresearch funds at land grant universities and stateagricultural experiment stations devoted to suchpractical matters as pest control are declining(66,307). Within the University of Californiasystem, for example, administrators recentlymoved to consolidate pest management pro-grams at the Davis and Riverside campuses.They began dismantling the agriculture depart-

10 The Experiment Station Committee on Organization and Policy is a subcommittee of a CSREES committee with representation fromevery State Agricultural Experiment Station.

ment at Berkeley, which included the oldest bio-logical control program in the country.

❚ State Agriculture DepartmentsThe states are involved in BBT research andimplementation through several routes. Theyprovide research matching funds for the StateAgricultural Experiment Stations throughCSREES and also directly fund experiment sta-tions and land grant universities for BBT work.Precise estimates of the direct funding areunavailable, but the amounts are probably signif-icant; state and private-sector contributions madeup 86 percent of total funding for the State Agri-cultural Experiment Stations in 1990 (154). Inaddition, a number of state departments of agri-culture have developed their own programs toresearch and implement biological controlagainst important pests affecting their states.These state government programs are the focusof this section.

In recent years, state departments of agricul-ture have been increasing their use of BBTs inintegrated pest management systems because ofconcerns about groundwater pollution, foodsafety, and pest resistance (228). Biological con-trol, in particular, now plays a key role. Cur-rently, 28 states have biological controlprograms, at a total annual cost of almost $10million (figure 5-2) (228). Several states main-tain insect-rearing facilities as part of theseefforts, although budget constraints have causedsome to close over the past four years; total statefunding declined by $2 million from 1990 to1994. California has the largest program; it ispart of an overall movement within the state toreduce reliance on conventional pesticides (box5-3).

State-funded BBT programs (most are appliedclassical biological control) generally workcooperatively with APHIS, the AgriculturalResearch Service, the Land Grant Universities,and the U.S. Fish and Wildlife Service (228). A

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m

HI7 programs*$1,070,000

FL5 programs*$1,125,000

* = maintains one or more rearing facilities● .

AK

SOURCES: Compiled by OTA from W.W. Metterhouse, Cream Ridge, NJ, “The States’ Roles in Biologically-Based Technologies for Pest Control,”unpublished contractor report prepared for the Office of Technology Assessment, U.S. Congress, Washington, DC, November 1994.

close relationship with APHIS results from com-mon regulatory responsibilities and the locationof APHIS operational staff within each state toassist with implementation programs. Statesdepend on APHIS to provide educational ser-vices and deliver materials for field implementa-tion (228). Once a released biological controlagent becomes established, however, it usuallybecomes the state’s responsibility to distributethe agent further, although sometimes APHIScontinues distribution when a state cannot (320).

Since 1966 there have been a number of suc-cessful federal-state biological control programs.Of the 28 states with biological control pro-

grams, 22 have cooperative efforts with federalagencies. Successful programs include cerealleaf beetle (Oulema melanopus), involvingUSDA, ARS, APHIS, and the states of Michiganand Indiana; Colorado potato beetle (Leptino-tarsa decemlineata), involving ARS and the stateof New Jersey; and the gypsy moth programs,involving ARS, APHIS, the Forest Service andseveral states (228).

❚ U.S. Department of the InteriorHistorically, the resource management agenciesof the U.S. Department of the Interior (DoI) con-ducted their own research to support manage-

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BOX 5-3: California Takes an Active Role in Changing Pest Management Practices

California is perhaps the nation’s leader in changing pest control practices and the adoption of BBTs.The state supports a diverse agricultural mix, with a significant emphasis on minor crops. Thus regulatory

restrictions on pesticides and declining availability of minor use chemicals are expected to hit the stateespecially hard. Innovations in pest control practices have also been driven in part by its health-con-

scious population. California has a long history of involvement with biological control and IPM; it was thesite of many of the most significant developments in the field, including the widely cited successful intro-

duction of the vedalia beetle (Rodolia cardinalis) to control cottony cushion scale (Icerya purchasi) in cit-rus.

The changes occurring in California reflect an overall effort within the state to shift away from a reli-ance on conventional pesticides. They are not haphazard; California has actively sought to develop stra-

tegic goals and policies to accomplish them.

The California Environmental Protection Agency’s program to regulate pesticides parallels that of theU.S. EPA. Its policies have an important influence on the decisions of pesticide manufacturers because of

the size of California’s potential pesticide market. The state now requires extensive reporting of pesticideuse. It also licenses pest control advisors, who must be college-educated in an agriculture-related field,

fulfill course requirements, and participate in continuing education. State regulators are currently consid-ering a proposed requirement that pest control advisors undergo four hours of training in the use of bio-

logical control and natural enemies.

The California Department of Food and Agriculture has the largest state program for biological control.It maintains an insectary for rearing natural enemies, and programs to implement biological control, cost-

ing about $1.3 million annually. Recent projects have addressed euonymus scale (Unapis euonymi),grape leafhopper, and water hyacinth (Eichhornia crassipes).

The University of California is home to an active statewide IPM program that is perhaps the best in thecountry at promoting pesticide alternatives, including BBTs. Funded partly through USDA, this program

sponsors hundreds of IPM research projects. It has been particularly effective at getting research resultsinto the field: Of the 180 research projects funded between 1979 and 1988, about 43 percent resulted in

pest control products or information that are now in use. A disproportionate number of the nation’sexperts in BBTs are on the faculty of the University of California, and many have collaborated with private

consultants and growers to develop innovative approaches using BBTs.

Farmers within the state have developed their own ways of promoting pesticide alternatives. The pub-lication Farmer to Farmer, written by and for farmers to share success stories in sustainable farming prac-

tices, originated in California. Regional organizations such as the Community Alliance with FamilyFarmers Foundation have worked with growers to develop biologically intensive farming practices such

as the use of natural enemies and other BBTs in almond orchards. Not surprisingly, many of the biggestnatural enemy companies are located in California.

SOURCES: C.M. Benbrook and D.J. Marquart, Challenge and Change: A Progressive Approach to Pesticide Regulation in Califor-nia, contractor report prepared for the California Environmental Protection Agency, Department of Pesticide Regulation (Sacra-mento, CA: April 1993); Community Alliance with Family Farmers Foundation, “BIOS: A New Project Promoting Biological AlmondFarming,” Davis, CA, 1995; J.I. Grieshop and R.A. Pence, “Research Results: Statewide IPM’s First 10 Years,” California Agricul-ture 44(5): September-October 1990; M.L. Flint, et al., Annual Report, University of California Statewide IPM Project (Davis, CA:University of California, September 1993); M.L. Flint and K. Klonsky, “IPM Information Delivery to Pest Control Advisors,” CaliforniaAgriculture March-April, 1989; T.L. Jones, Special Assistant to the Director, Department of Pesticide Regulation, California Envi-ronmental Protection Agency, Sacramento, CA, personal communication, U.S. Congress, Washington, DC, July, 1995; W.W. Met-terhouse, Cream Ridge, NJ, “The States’ Roles in Biologically-Based Technologies For Pest Control,” unpublished contractorreport prepared for the Office of Technology Assessment, U.S. Congress, Washington, DC, November 1994.

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ment functions. This arrangement changed withthe formation of the National Biological Service,the newly consolidated research arm of thedepartment that was established in November1993 by an order of the Secretary of Interior.11

The National Biological Service inherited asomewhat mixed portfolio of BBT-relatedresearch programs. Most of these had grown outof specific concerns of federal land managersrather than any overarching program or statedgoal to implement BBTs. For example, theNational Biological Service is studying insectsand fungi as potential controls for non-nativeinvasive plants for the National Park Service andthe Fish and Wildlife Service. Past efforts haveincluded working with USDA and the NationalPark Service to evaluate bacteria for control ofgypsy moth (427). Other related researchprojects are evaluating waterfowl and fish preda-tion as potential controls for zebra mussel (Dre-issena spp.), several species of flea beetle forcontrol of leafy spurge, and several weevil spe-cies for control of purple loosestrife (Lythrumsalicaria) (427). Expenditures by DoI on BBTresearch totalled around $1 million in fiscal year1994 (181). This figure includes $85,000 to$100,000 in funds from the Bureau of Land Man-agement “passed through” to help support theARS weeds lab in Bozeman, Montana (290).

The Department of the Interior has only a fewpest control programs using BBTs. These pro-grams are scattered haphazardly throughout DoIwithin at least four resource management agen-cies. The Bureau of Land Management uses bio-logical control on weeds in nearly all of theWestern states. The weed targets include fieldbindweed (Convolvulus arvensis), gorse (Ulexeuropaeus), poison hemlock (Conium macula-tum), diffuse and spotted knapweed (Centaureadiffusa, C. maculosa), yellow starthistle (Centau-rea solstitialis), leafy spurge, and purple loose-strife. The lack of greater emphasis on BBTswithin DoI is somewhat surprising, given the

11 CFR Vol.. 58, No 229 December 1, 1993, 63387.

technologies’ potentially high compatibilitywith management of environmentally sensitiveareas. It may, in part, reflect the historical lack ofemphasis on pest management among federalland management agencies (338). The result hasbeen a growing belief among many managersthat pests of natural and less managed areas—specifically nonindigenous species that kill, con-sume, parasitize, or compete with native spe-cies—are now significant threats to thebiodiversity and continued value of these naturalresources (338).

A number of DoI agencies are members of theFederal Interagency Committee for the Manage-ment of Noxious and Exotic Weeds mentionedearlier in the chapter (303,388). This group arosein response to new requirements in the 1990Farm Bill12 that all federal land managersdevelop programs for control of “undesirableplants.” In addition, concern had been growingfor some time among staff within the Bureau ofLand Management that noxious weed problemswere rapidly outstripping the Bureau’s ability tomanage them with conventional methods. Theinteragency group has representatives from fouragencies in the USDA: the Forest Service, ARS,APHIS and CSREES; six agencies in DoI: theNational Park Service, the Bureau of Land Man-agement, the Fish and Wildlife Service, theNational Biological Service, the Bureau of Rec-lamation, and the Bureau of Indian Affairs; theDepartment of Defense; and several other agen-cies. Among this group’s stated goals is toincrease the necessary research to discover anddevelop biological control agents for weed con-trol (388).

DoI initiated several related efforts in 1995.The Secretary of the Interior designated a newtask force to address noxious weeds specificallyon DoI lands and issued a secretarial orderrequesting that DoI bureaus develop coordinatedweed prevention and management strategies(290,303). The departmental manual’s guidance

12 The Food, Agriculture, Conservation and Trade Act of 1990, P.L. 101-624.

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on weed control was revised, and now specifiesincorporation of integrated pest management,including biological control, into weed controlprograms. The revised guidance also establisheda committee to coordinate DoI weed controlactivities and instructed the National BiologicalService to provide scientific information andresearch support for the DoI weed programs,including development of integrated weed man-agement systems (303).

❚ Army Corps of EngineersThe Army Corps of Engineers has had a researchprogram on biological control of noxious andnuisance aquatic weeds since 1959, funded ataround $1 million for the past few years. In coop-eration with USDA, the Corps conducts researchto identify natural enemies for weeds that impedenavigation, restrict water flow, and dominate thenatural system by the formation of single speciesstands. In the 36 years of joint research, theCorps believes that the program has beenextremely successful. Scientists have released 12biological control agents for the management offour plant species, including alligator weed(Alternanthera philoxeroides), water hyacinth,water lettuce (Pistia stratiotes), and hydrilla(Hydrilla verticillata). These programs cover 15states. Corps scientists have also been involvedin evaluating three potential pathogens for weedcontrol. Aside from ARS collaborators, no oneelse in the federal government conducts similarwork to address aquatic weeds.

Through the Department of Defense’s mem-bership in the Federal Interagency Committee forthe Management of Noxious and Exotic Weeds,scientists from the Corps’s aquatic weed pro-gram have recently become involved in develop-ing systems to enhance implementation of weedcontrol programs using BBTs and other methods(51). One project under way is the constructionof a database of ongoing research on weed con-trol. The other is development of an expert sys-tem that will eventually provide users withinformation on various options for controlling

specific weeds, constraints on the use of thesemethods, and their effectiveness.

The Clinton Administration proposed elimi-nating the approximately $10 million budget forthe Corps’s aquatic weed program in its fiscalyear 1996 budget proposal. As of August 1995,the fate of the program was as yet undecided inCongress.

❚ Environmental Protection AgencyThe Office of Research and Development of theU.S. Environmental Protection Agency (EPA)administers a research program to provide riskassessment tools. These research activities areundertaken in part to assist the EPA’s Office ofPrevention, Pesticides, and Toxic Substancesduring pesticide registration, special review, andreview of premanufacture notices submitted byindustry (107). EPA’s research focuses primarilyon microbial pesticides. Its purpose is to assist inmaking sound evaluations of the risks and bene-fits of microbial pesticides, including those basedon bacteria, fungi, and viruses, and certain genet-ically modified organisms (398). Funding formicrobial pesticide research at three EPA labora-tories totaled $684,600 for fiscal year 1995. Itincluded cooperative field studies with universi-ties regarding the potential fate of microbial

The Army Corps of Engineers program for biological control ofaquatic weed, such as water hyacinth (Eichornia crassipes) isone of two weed control programs slated for elimination in thecurrent round of federal budget proposals.

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agents and their effects on terrestrial environ-ments, food web interactions, ecosystem func-tions, freshwater populations, and nontargetmarine and estuarine animals (107).

❚ Other Federal Sources of FundingThe National Science Foundation and theNational Institutes of Health provide a smallamount of funding for BBT research, primarilyon the natural enemies of arthropods and behav-ior modifying chemicals (247). Between 1989and 1993 the National Science Foundationawarded an average of $1.5 million annually forresearch on biological control, and a total of$388,000 for research on behavior-modifyingchemicals. The agency also provided severalgrants for studies of the systematics of parasiticHymenoptera (a taxonomic group that contains anumber of biological control agents). In 1993,the National Institutes of Health awarded$500,000 for biological control research andclose to $1 million for research on behavior mod-ifying chemicals (247).

Funds from several small programs of USDAalso are potentially available for BBT research,although researchers have been somewhat disap-pointed in the level of BBT work supported bythese programs (247). The Small Business Inno-vation Grants program funded one to three bio-logical control programs per year between 1989and 1992. The Alternative Agriculture Researchand Commercialization center, whose charge isto aid in the commercialization of agriculturalproducts for industrial use, contributed $170,000to develop a microbial pesticide based on Bt in1993. That same year, USDA’s SustainableAgriculture Research and Education programfunded two biological control projects.

The Interregional Research Project No. 4(“IR-4”), funded by CSREES and ARS, carriesout the necessary research to supply datarequired for registration of pesticides (includingmicrobial pesticides and pheromones) for use onminor crops. Over the 10-year period followingthe program’s expansion in 1982 to cover “biora-tional” products, it supported research projects

on 13 microbial agents (130). BBTs representonly a minor component of the program; mostfunds go to research on conventional pesticides(247).

EDUCATING USERSIn addition to direct administration of researchand implementation programs, federal and stateagencies affect the adoption of BBTs by farmersand other users. The major institutions involvedare the Cooperative Extension Service and LandGrant University system. Decisions of users toadopt BBTs also may be influenced by producestandards, and other legal and financial mecha-nisms. Today, private consultants play anincreasingly important role in pest control deci-sions, sometimes far surpassing that of govern-ment programs. This section begins by exploringfarmers’ perspectives and then examines some ofthe factors that influence their adoption of BBTs.

❚ The Farmers’ PerspectiveMost farmers have little or no information on theefficacy, quality, economic feasibility or otheraspects of BBTs (141,270). Even farmers whouse these technologies often lack clear-cutinstructions on how to apply them. Many BBTsare labor-intensive and their optimal use requiresa significant amount of information (59) (seechapter 3). Few farmers will embrace technolo-gies that seem to involve many inexact proce-dures and unknown consequences (6,240).

Farmers also lack information on their spe-cific pest control options (271). Growers needinformation on what BBTs are available and howto obtain the best results using the technologies.Such information—custom-designed for the tar-get audience and specific to the local crop, pest,and environmental conditions—is usuallyunavailable (79,253). In a survey of organicfarmers, about 60 percent said existing informa-tion sources failed to meet their needs (260). Inmany cases such information has never beendeveloped (292). Implementation of even themost effective BBTs suffers when the base ofresearch on their application is inadequate.

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Some of the well-known advantages of BBTs(e.g., superior environmental profiles, and lowersusceptibility to resistance) accrue to the broaderagricultural community rather than to the indi-vidual grower. Farmers may wonder whether it istruly in their personal best interest to switch toBBTs. Of more immediate concern to most farm-ers are the effectiveness, cost, and demonstratedsuccess of the product, as well its ease of applica-tion, safety, compatibility with natural enemies,and other factors (49,114,135,179,213). Unlikeconventional pesticides, many BBTs cannot beapplied across wide areas with the expectation ofconsistent results (see also chapter 3) (253).

Despite their pragmatic concerns about cost-effectiveness, many farmers would prefer to useless chemical-dependent technologies (101).They are prompted in part by consumer demand,the development of pesticide resistance, thedeclining array of registered pesticides, eco-nomic considerations, and the growing aware-ness of the effects of chemical pesticides on localgroundwater supplies. Environmental and occu-pational health concerns play a role as well. A1992 study of 297 fruit growers in Michigan, forexample, found that less than 1 percent plannedto increase pesticide use, while 61 percent saidthey would decrease pesticide use in the futureby adopting IPM or organic techniques (231). Insome cases the use of BBTs and other IPMapproaches has resulted largely from economicconsiderations. These practices sometimes proveeconomically superior to conventionalapproaches (238), for example, when pestsbecome uncontrollable due to resistance or whenpesticide use (and therefore costs) can bereduced through IPM.

Use of some BBTs has become widespreadpractice in certain crops and geographic regions(see chapter 3). In Florida a majority of cabbagegrowers use Bt rather than conventional pesti-cides against diamondback moths, because theywant to conserve natural enemies such as ladybeetles and lacewings (213). Florida growersoften use pheromones as a scouting tool, but less

frequently for trapping pests given the high costsof this technique. Roughly 30 to 40 percent ofFlorida strawberry farmers release predatorymites to control spidermites, and many citrusgrowers rely on parasitic wasps to control citrussnowscale (Unaspis citri) (213).

In California nearly 300,000 acres of citruswith low pest abundance have been set aside asbiological control zones. Growers follow cropmanagement practices that conserve the nativenatural enemies, and they also augment the bio-logical control populations when necessary.According to the California Citrus ResearchBoard, such orchards can be highly cost-effec-tive, relying on natural enemy populations builtup over many decades (18). But they are precari-ous arrangements; for example, natural enemypopulations that had been built up over half acentury in one Corona (California) orchard weredestroyed by mass-spraying of malathion againstthe Mediterranean fruit fly (Ceratitis capitata).The growers subsequently abandoned theorchard (18).

Even a number of more prominent firms areinterested in diversifying their pest control tech-nologies (see figure 3-1 in chapter 3). The DoleCompany rears predatory sixspotted thrips (Sco-lothrips sexmaculatus), while the Gallo Wineriesuse Trichogramma wasps, green lacewings, andpredatory mites (270). The goal of Fetzer Vine-yards is to produce or buy 100 percent organi-cally grown grapes by the year 2000 (94).Campbell Soup Company has nearly eliminatedthe use of synthetic insecticides on its processingtomatoes in Sinaloa, Mexico, using pheromones,Trichogramma wasps, and Bt (38). Campbell’sIPM efforts (box 5-4) show that IPM is feasibleand even profitable on a crop for which somecompanies consider non-conventional methodsneither promising nor practical (137).

For some crops and pest control needs, how-ever, few BBT options exist. According to oneblueberry growers’ marketing cooperative inMichigan, commercial buyers do not tolerate anyevidence of pest activity—a standard that few

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BBTs can attain (see also chapter 3) (331). Con-sequently, the only suitable BBT presently avail-able is Bt for use against cranberry fruitworm(Acrobasis vaccinii) and leaf rollers. Growerswould like more BBT options, particularly formajor pests such as blueberry maggot (Rhagole-tis mendax), Japanese beetles (Popillia japon-ica), and the many diseases affecting blueberries(331).

❚ Technology Transfer to End Users

The Government’s Role Through ExtensionThe principal governmental provider of direct,hands-on assistance to growers is the Coopera-tive Extension Service. The system is made up offederal personnel at the USDA Cooperative StateResearch, Education, and Extension Service(CSREES), as well as state and county-levelagents. These components are often loosely

BOX 5-4: Campbell Soup Company

Campbell Soup Company has dramatically reduced its reliance on conventional pesticides in certainregions by adopting IPM systems that incorporate BBTs, field scouting, and disease monitoring. The

company employs its own in-house IPM specialists who conduct field research and put the programs inplace.

Campbell’s most active IPM efforts take place in tomato farming. The company has nearly eliminatedsynthetic insecticide usage and has reduced fungicide application by more than 50 percent in its pro-

cessed tomato operations in Sinaloa, Mexico. Growers use Bt to control armyworm; Trichogramma waspsto control tomato fruitworm (Helicoverpa zea); and synthetic sex pheromones to disrupt the mating of

tomato pinworms (Keiferia lycopersicella). Other IPM techniques include: selecting fields and plantingtimes to minimize risks of virus diseases that are transmitted by whitefly pests; monitoring pest and natu-

ral enemy abundance using pheromone traps and scouting; and using a computerized disease forecast-ing system that tracks hourly temperature and leaf-wetness to pinpoint when to spray fungicides to

control late blight. Taken together, the IPM programs in Sinoloa save an estimated $400 per hectarewhen compared to conventional pesticides.

Campbell Soup encourages its U.S. tomato growers to use IPM, but the level of adoption trails its Mex-

ico operations. Comparison of the company’s operations in Sinaloa and California illustrates how loca-tional differences—such as labor costs, infrastructure, and pest pressures—can affect adoption of BBTs

and IPM. In Mexico, the company conducts monitoring and other IPM activities for the grower, while inCalifornia, the choice of pest control method rests with the individual farmer. The company encourages

California growers to reduce pesticides and offers education programs. Campbell Soup also demon-strates BBTs and other IPM techniques in growers’ fields, with the company assuming all financial risks

for drops in yield during the experimental period. In Mexico, low labor costs make more labor-intensivetechniques cost effective, such as those involving pheromone dispensers, natural enemies, and scout-

ing. Also, the absence of native natural enemies in Sinaloa makes augmentative releases essential; innorthern California the native natural enemies partially protect tomatoes against fruitworm and other

regional pests.

Campbell Soup Company relies heavily on land grant universities and extension in developing its IPMprograms and educating California growers. The company actively seeks out researchers whose work is

relevant and provides small grants to direct their attention to particular issues.

SOURCES: H.A. Bolkan, “Campbell Soup Company Integrated Pest Management,” IPM Monitor, Summer, 1994; Campbell SoupCompany, Integrated Pest Management Research and Implementation, “Economic Profitability and Environmentally CompatibleAlternatives,” Products and Progress Report 1994–1995; R.K. Curtis, Campbell Soup Company, Sacramento CA, letter to Edu-ardo Martinez Curiel, Consul of Mexico, February 1, 1994; R.K. Curtis, Campbell Soup Company, Sacramento, CA, personal com-munication, Summer 1995; P. Marrone, President, Novo Nordisk Entotech, Davis, CA, personal communication 1995.

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coordinated through the land grant colleges.Extension is represented in nearly all of thenation’s 3,150 counties (342). However, privatepest control consultants seeking assistance insolving difficult pest problems frequently bypasscounty agents in favor of the more technicallyeducated state specialists (412). Each state runsits extension program differently. In Vermont,for example, all extension is closely tied to thestate university, while in New York State eachcounty runs its own program, even though all areofficially under the umbrella of the CornellCooperative Extension (121).

Although extension programs historicallyplayed a key role in farmers’ pest control deci-sions, today this role is minimal in most states(114). In general, the Cooperative Extension Ser-vice is financially strapped and the workforcespread thin among multiple responsibilities,ranging from programs aimed at preventingpregnancy and drug use, to nutrition educationfor low-income families. Despite the recentretirement of many “old guard” extension agents,who entered the land grant colleges after WorldWar II and were trained in conventional pestcontrol, the more recently educated and, in somecases, IPM-oriented agents may have only lim-ited opportunity to bring nonchemical practicesto the field (98,166).

Most extension agents have had little if anyformal exposure to biologically basedapproaches (207). The relationship between theAgricultural Research Service and CooperativeExtension is a distant one (114), and many of theextension-affiliated land grant colleges offer atmost minimal training in BBT use.

Moreover, in many parts of the country, thelimited amount of research on applications ofBBTs provides little locally generated andregionally relevant information (97,207). Conse-quently extension specialists often do not havemany “field-ready” BBT options. They also lackthe resources to do the applied research neededfor implementation. Many extension personnelfeel caught in the middle between a clientele whoasks for pesticide alternatives and a research

pipeline that fails to deliver effective, ready-to-use technologies (180).

This inadequacy helps explain the lack ofdetail found in most of the educational materialsproduced by the 27 states that support biologicalcontrol as part of their IPM programs (97). Asmall, informal survey of randomly selectedstates in the Northeast, North Central, South andWest found tremendous variation among thestates in their extension publications’ educationalvalue to growers regarding BBTs (247). Of the13 states sampled, New York consistently toppedthe ratings; it was the only one having extensionmanuals devoted solely either to natural enemiesor to pheromones (247). Another small surveythat evaluated extension publications from theNorth Central states concluded that the coverageis usually too perfunctory to provide the skillsnecessary to adopt biological control (207).

In fiscal year 1995, CSREES received approx-imately $14 million in appropriations for exten-sion work in IPM research and implementation.It is uncertain whether increases in this area pro-posed under the USDA IPM Initiative for fiscalyear 1996 will occur (see box 5-1). In contrast, atleast in certain regions of the country, extensionscientists expect increased responsibilities in thisarea; according to a 1994 survey of 38 extensionentomologists in North Central states, mostspend slightly more than 10 percent of their timeon classical biological control programs, but theyexpect this percentage to triple over the nextdecade. Most of the agents also reported anincrease in questions from growers about biolog-ical control and pesticide reduction (207).

Private Pest Control AdvisorsIn most regions, the Cooperative Extension Ser-vice now plays a role that is secondary or inter-mediary to that of the private informationsources such as pesticide dealers, pest controladvisors, crop consultants, and pesticide applica-tors (253). Extension agents may develop dem-onstration projects and training activities forgrowers and commercial crop consultants, andsometimes they validate private sector recom-mendations or investigate unusual pest out-

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breaks. But most growers rely far more onprivate sector advisors than on government agri-cultural experts (253). The lack of funding forextension activities at universities has strength-ened the private pest management business(270). Often the Extension agents are far out-numbered by private advisors (291). Large farmoperations, which can spread the cost of obtain-ing information over more units of production,depend particularly heavily on private consult-ants and can afford to hire the very best (see box5-4) (141).

Most private advisors have been educatedwith an orientation toward conventional pesti-cides. Most are not well versed in biologicallybased methods—around 5 percent, according tosome natural enemy companies (269). The extentto which advisors use BBTs varies tremen-dously; some are eager to embrace these technol-ogies but do not have adequate information orfind that few biological approaches suit their pestcontrol needs. Some advisors lack confidence inthe BBT options and do not want to harm theirreputations by recommending a technology thatthey themselves question (282).

Moreover, most private pest control advisorsare affiliated with the chemical industry. Thereare also about 3,500 “independent” consultantswho do not work for chemical suppliers (340). InCalifornia, for example, about 200 (less than 10percent) of the pest control advisors who areactive in agriculture are considered independent;the rest work for chemical companies, distribu-torships and applicators (141). In a few states,such as California, Arizona and Florida, some ofthe pest control advisors specialize in BBTs(435). Independent consultants charge growers afee, averaging from $3.75 per acre for wheat to$17.40 per acre for vegetables (340), whereasthose affiliated with pesticide companies offerfree advice as an incentive for product purchases.

Independent consultants may be more inclinedthan industry-affiliated advisors to recommendnonchemical technologies. A study of pest con-trol advisors in California found that those notinvolved in the sale or application of pesticideswere much more likely to seek help from the

extension personnel than from pesticide com-pany representatives or other informationsources (102). A 1994 nationwide survey of thefarmers under contract with independent consult-ants found that 20 percent of the vegetable grow-ers were releasing beneficial insects and 39percent were using pheromones (340)—rates ofuse substantially higher than the national aver-ages (e.g., ref. 377).

Few states have licensing requirements forprivate pest control advisors (309). Many advi-sors are, however, certified by professional soci-eties such as the American Society of Agronomyand the National Alliance of Independent CropConsultants (7,16,166). The societies have devel-oped certification standards to eliminate the needfor government intervention. These standardsvary among states. No state government requirespest control advisors be trained specifically inBBTs (5), although such training has been pro-posed in California (see box 5-3). Likewise EPAhas no certification requirements for private pestcontrol advisors and offers no guidance to thestates in this area (431).

EPA does annually pass through about $2million to CSREES for development of modelcurricula for training pesticide applicators (370).These curricula suggest including a section onIPM, although very little specificity is includedregarding what techniques might be covered. Thecurriculum, with modifications related to statelaws, is used by the Cooperative Extension Ser-vice in all states to annually train over 500,000private, commercial, and urban pesticide applica-tors (370). Under the Federal Insecticide, Fungi-cide and Rodenticide Act, however, EPA isbarred from requiring IPM training for licensingof pesticide applicators. Pesticide applicatorsunfamiliar with BBTs might pose an obstacle togrowers interested in experimenting with thesetechnologies.

❚ Other Factors Affecting the User’s ChoiceA number of institutional factors and market-place forces may also affect farmers’ pest control

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decisions. The precise influence of most has notbeen rigorously documented. For example, themarket for foods grown with reduced or no pesti-cide use, and the prices consumers are willing topay for these foods, may affect whether and howgreat a cost farmers are willing to incur inswitching to pesticide alternatives. Bankers whoare unfamiliar with IPM or BBTs and who per-ceive the methods as presenting a higher risk ofcrop failure may be unwilling to approve agricul-tural loans to farmers who use these methods(435). Some growers worry that use of IPM andBBTs may be impeded by the new Worker Pro-tection Standards recently issued by EPA thatincrease the amount of time after pesticide appli-cation during which agricultural workers arebarred from reentering fields. The required delaywill prevent growers and crop consultants fromreentering fields shortly after spraying to scoutfor remaining or fresh pest populations; somegrowers argue the lack of immediate monitoringwill force them back to calendar spray schedules(31).

Perhaps the most commonly discussed influ-ence is cosmetic standards. Federal, state, andprivate grading standards for specific attributessuch as the shape, color, and surface defects offruits or vegetables may also drive certain pestcontrol decisions. USDA grades for fresh fruitsand vegetables, commonly specified in businesscontracts, are required under some federal mar-keting orders establishing minimum standards, aswell as for produce sold to the federal govern-ment and for certain commodities imported andexported (380). Most retailers buy only produceof the highest USDA grades to ensure adequateappearance (297). In addition, some states havestandards for certain crops, and many firms, suchas Sunkist, have private standards for fresh pro-duce. The failure to meet particular grading stan-dards can lead to downgrading or to loss ofaccess to the fresh market altogether, and conse-quently a substantial loss of income (298).

Produce standards in many fruit, vegetableand nut crops are also affected strongly by exportmarkets. For example, about 40 percent of Cali-fornia citrus is destined for Asian and European

consumers. Cosmetic standards for these marketsare far higher than those in the United States,making use of conventional pesticides almostunavoidable for produce intended for export(18).

The extent to which growers use conventionalpesticides to meet cosmetic standards remainscontroversial, however (189,298,380). Somestudies suggest that a grading system whichemphasizes external appearance may leavegrowers and packers little choice but to applylarge amounts of conventional pesticides. Somesurveys of apple and citrus growers report, forexample, that for a majority of growers at leasthalf of their pesticide usage is to attain a suitablecosmetic appearance (298). Although citrus is acrop that lends itself well to BBTs (18), in partsof California no BBT can fully control the thripand red scale pests responsible for cosmeticblemishes. Fruit going to the processed marketsometimes has been treated with the sameamount of conventional pesticide as that going tothe fresh market by growers hopeful that most oftheir fruit crop will be accepted in the fresh mar-ket (92,298).

Production arrangements vary in the extentto which they direct the grower to useparticular pest management approaches; mostonly require that the final product meets certainstandards, although some are quite specific(21,83). In general, processors are more likelythan fresh commodity buyers to specify thedesired pest control method in a grower agree-ment or contract (213). However, the degree ofproducer control can vary greatly, even within aparticular crop for a particular use. The variationreflects differences among growers and firms inmanagement skills, access to credit, and riskpreferences (435). For example, three Californiafirms handle more than 75 percent of US freshcarrot production. Their production arrange-ments with growers range from some that givevirtually complete control over pest control, toothers that cover only the purchase of output.

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FROM RESEARCH TO IMPLEMENTATIONChapter 5 has shown that the federal governmentsupports sizable efforts on the research andimplementation of BBTs, funded annuallyaround $210 million. Despite these efforts, appli-cations of BBTs in the field are relatively few(chapter 3). And a significant gap lies betweenthe research on BBTs and its use—a gap referredto by some long-time observers as the “valley ofdeath.” The problem characterizes BBTs in othercountries as well (e.g., box 5-5). Here OTA iden-tifies some of the major reasons for

this chasm and suggests options that might helpprovide solutions.

❚ Coordination Is Needed to Enhance Delivery to the FieldA lack of necessary coordination betweenresearch and implementation was the most prom-inent problem identified by every workshop andadvisory panel convened during the OTA assess-ment, and by dozens of scientists and representa-tives of federal agencies. The issue is not simple;

BOX 5-5: Connection between Research and Implementation in Australia

U.S. scientists often point to Australia as a potential model for the United States to emulate in the reg-ulation of biological control. It is unclear, however, whether differences between the U.S. and Australian

regulatory systems have had a significant impact on the relative adoption and success rates of biologicalcontrol or other BBTs. Although Australia is thought to be several steps ahead of the United States, both

its research and its implementation efforts appear to confront many of the same obstacles plaguing U.S.programs—most notably, low rates of success, adoption, and commercialization. Despite regulatory

developments, discontent about the screening and approval process for introductions remains prevalent.

The Australian government has instituted several national policy initiatives that have removed some ofthe regulatory obstacles that American scientists and natural enemy companies claim inhibit the success

of biological control in the United States. The result, however, has not been greater use or commercializa-tion of BBTs. A series of complete and partial successes have kept BBTs in the public eye and in

demand, but private-sector involvement remains minimal. Research results are not getting into the com-munity for widespread use, and the Australian government has been ambivalent in its attempts to

improve the situation.

In 1989 the Australian government spent only a small percentage of its pest control research budgeton BBT research and implementation—$20 million, an amount equivalent to approximately 2 percent of

the funds spent on chemical research. Although there is widespread acceptance of the need to encour-age BBTs, there is little in the way of explicit directives, and resources are still limited. The government

does not give any subsidies to encourage BBT use, and support for redistribution of biological controlagents and implementation projects and resources is still inadequate. The only potential government

incentive for growers to adopt BBTs is the increasing restriction on conventional chemical pesticides.This incentive may eventually become strong, but it has not yet had much impact on growers.

The Australian government has several policies that help link research to implementation. One of the

conditions of government funding is that recognition be given to the importance of long-term researchand research for public benefit. Consequently, Australian scientists often integrate the implementation

phase with the initial research. Both the central government and the state governments encourageresearch agencies to promote their work on BBTs more publicly. Nevertheless, farmers and researchers

alike realize that the results are not getting out to the field.

SOURCE: J.M. Cullen, and T.E. Bellas, Division of Entomology, CSIRO, Canberra, Australia, “Australian Laws, Policies, and Pro-grams Related to Biologically Based Technologies for Pest Control,” unpublished contractor report prepared for the Office ofTechnology Assessment, U.S. Congress, Washington, DC, March 1995.

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this need for coordination occurs on several lev-els. In general, ad hoc interactions among scien-tists from various government agencies anduniversities working on BBTs have been quitegood. Problems arise, however, when institu-tional coordination is necessary.

Interdepartmental CoordinationIn the 1990 Farm Bill, Congress directed EPA tocoordinate with USDA in identifying pressingnational needs where shortages in pest controlmethods are likely to occur through the loss ofconventional pesticides. The most obviouscauses of such shortages are the lack of reregis-tration of chemicals for minor use crops and pes-ticide resistance (see chapter 2). USDA wasinstructed to address these priorities through itsresearch and extension programs.13 In 1994, theSecretary of Agriculture and the Administratorof EPA signed a memorandum of understandingbelatedly agreeing to collaborate in exchangingnecessary information on upcoming pesticidelosses (403).

OTA has not been able to identify any clearmechanism by which such priorities are consis-tently identified and acted upon in the develop-ment of the portfolio of USDA-funded researchon BBTs. The first step would be to improve theinformation exchange between USDA and EPA.

Congress could, through its oversightfunctions, encourage USDA and EPA to act on theirrecent memorandum of understanding.

Congress could specify and providedirect appropriations (perhaps as a proportion of thefunds requested for the USDA IPM Initiative) for USDAand EPA to collaborate in developing and maintaininga database on upcoming pest control needs (result-ing from pesticide loss and resistance) and availablealternatives for filling these needs. Careful consider-ation would need to be given to the appropriate insti-tutional site for this function; the database wouldrequire sustained support. It should be constructed toensure universal accessibility and also so that it can

13 Under the Conservation and Research Titles of the 1990 Farm Bill.

provide guidance for the funding decisions ofresearch agencies.

In December 1994, Argonne Laboratories, undercontract with the Cooperative State Research, Educa-tion, and Extension Service began developing thesoftware for a database that would incorporate stateinformation on the use of various pest control methodsand EPA data on pesticide reregistration (289).CSREES hopes the database will one day includeinformation on pesticide resistance and USDAresearch, and that it will eventually be supported bystates and users. Should Congress decide to desig-nate this database as the national repository of infor-mation on pending pest control needs, some earlyadjustment might be needed to make sure it fulfills thecriteria just discussed. For example, CSREES shouldconsult with the Agricultural Research Service andother agencies to ensure that the database is con-structed so that it can inform their decisionmakingregarding research priorities.

Providing for Follow-Through in the ResearchThe Agricultural Research Service (ARS) and theState Agricultural Experiment Stations fund mostof the research on BBTs. In both cases, the sci-ence usually is generated “bottom up.” Nationalgoal-setting mechanisms lack funding authorityand therefore have little direct influence over theresearch agenda. The decision processes of ARSand the State Agricultural Experiment Stationshave the advantage of keying research to region-ally identified problems. Where they fall down,however, is in their ability to address externallyidentified strategic needs. This is particularly aproblem for work on BBTs. A vast array of pestmanagement questions deserve scientific investi-gation. The diffuse mechanisms for generatingresearch projects and the limited funds availablecannot help but result in a research portfolio thatis dispersed and lacks coordination.

One consequence of the scatter is that some ofthe research components necessary to enable thepractical uses of BBTs are not addressed. Theapplication of any given BBT against a specificpest problem results from research ranging from

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fundamental aspects of the pest problem todetails of how the BBT is applied.The latter has consistently been underempha-sized. OTA fully acknowledges the value ofmore fundamental research and is not addressingwhether the current allocation here is appropri-ate. But it is clear that not enough attention hasbeen given to the essential research to take BBTsout of the hands of scientists and into those offarmers and other users. Historically,no research agency has identified this function as itsresponsibility. Extension scientists might have beenlogical candidates but have not assumed this role(84).

Another consequence of the funding processesof the ARS and the State Agricultural Experi-ment Stations is that the agencieshave difficulty responding to exter-nally generated research needs, such as thoseidentified by operations agencies. Despite clear-cut institutional responsibilities, ARS has notalways delivered solutions that are field-ready toAPHIS; as a result, APHIS has developed itsown research capabilities for adapting BBTsoriginally identified by ARS and others forlarger-scale field use. Similarly, the needs of theland management agencies for BBTs to use inweed control have been met only by a small scaleeffort at ARS, even though weed-infested landsare extensive and represent a significant nationalproblem. In part, this reflects the fact that agen-cies within the Department of the Interior(DoI)—the Bureau of Land Management in par-ticular—lack pass-through funds that they couldallocate to ARS for the related work. Futureneeds of the DoI agencies may be particularlyacute because their research agency, the NationalBiological Service, lacks support in the currentCongress and has been targeted for downsizing,elimination, or merger.

The difficulty that USDA’s major researchagencies have in responding to externally identi-fied priorities does not bode well forhow the agencies will deal with impending pesti-cide losses through reregistration or pesticideresistance, even if this information is madereadily available through better coordinated

efforts with EPA. This has special significancefor BBTs because these technologies are mostlikely to be adopted where conventional pesti-cides disappear (see chapters 3 and 6).

Experience has shown that research flowsmore expeditiously into applications of BBTswhen directed funds circumvent the normal,highly structured, institutional processes. OTA’soptions attempt to build on this experience.

Congress could direct the AgriculturalResearch Service to allocate a proportion of its BBTfunds to a targeted competitive grants program withinthe agency. These funds would be available for col-laborative research projects that provide the followthrough into field applications. Evaluation of theneeds of farmers or other users at the inception of theresearch and of ways in which the BBT would meetthis need would be essential to ensure real-worldapplicability. The size of this effort would need to bebalanced against its potential effects on the agency’scapability to conduct longer-term studies.

Proposed research funding for fiscalyear 1996 provided through CSREES under the USDAIPM Initiative has taken this approach to ensure “buyin” by researchers, farmers, and others involved in allphases of the development and implementation ofIPM programs (see box 5-1). Congress could fundthis research initiative. Its potential influence on BBTresearch is unclear, however, because the role ofBBTs in the IPM Initiative has not been explicitlystated. Hence, funding of the research component ofthe IPM Initiative would affect BBTs only if Congressinstructed USDA to identify the role of BBTs or to allo-cate a proportion of the program for IPM research thatincorporates biologically based approaches (i.e., bio-intensive IPM).

Congress could increase the account-ability of the Agricultural Research Service to theoperations and land management agencies by desig-nating funds within these agencies for pass-throughto ARS for meeting their operational needs. Becausenew funding is unlikely in the current fiscal climate,these funds would have to be derived from the currentbudgets of these agencies.

Alternatively, Congress could allocateto the operations and land management agencies“redeemable credits” toward research that targets

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their needs by the USDA research agencies. Thesecredits would obligate the research agencies to con-duct a specified amount of research to meet theneeds of the operations and land management agen-cies, but no exchange of funds would occur (i.e.,funds would remain in the research agencies). Theresearch agencies would have to be informed, duringtheir appropriations processes, of their obligations,and some tracking mechanism might be necessary toassure accountability for conducting the work andproducing results according to the agreed priorities.

Congress could improve the matchbetween ongoing research and the needs of farmersby requiring research agencies to seek input fromfarmers and other users into funding decisions. Forexample, representatives of user groups, commoditygroups, etc., could sit on funding panels or make rec-ommendations to the Deputy Administrator of theNational Program Staff of the Agricultural ResearchService.

Congress could create a competitivegrants program specifically targeted toward BBTsthat are well researched but not yet in practical use.The goal would be to invest in bringing research dis-coveries that currently lie unused into the field, partic-ularly those of high technical merit but likely to yieldprofits too low to be of commercial interest. Suchfunds might be administered through CSREES, per-haps as a part of its extension functions. Althoughnew money would be required to set up the program,it would be very cost-effective, because only technol-ogies on the verge of application would be funded.The same type of targeted funding mechanism cur-rently underlies the Cooperative Research and Devel-opment Agreements under which private-sectorcompanies invest in government research (see alsochapter 6 for further options related to CRADAs).However, those agreements primarily addressresearch that is amenable to commercial develop-ment.

Coordination of Biological ControlCoordination of biological control research posesseparate but related problems. Researchers pointto dwindling resources and institutional obstaclesas significant reasons why current rates of suc-cess in classical biological control are low (58)(see chapter 3). At the same time, the numbers of

people and organizations conducting biologicalcontrol are growing ever larger. Numerous smallcompanies also rear and sell natural enemies (seechapter 6). In the past, scientists at the Agricul-tural Research Service and universi-ties conducted most biological controlintroductions. Today, federal, state, and countygovernment agencies responsible for pest controlcarry out their own programs, often in the rush ofaddressing a new, high-cost pest, such as theRussian wheat aphid.

Research scientists worry that the quality ofbiological control work will suffer as it becomesincreasingly dispersed. The conse-quences might include increasedintroduction of ineffective agents, greater poten-tial for introduced agents to interfere with oneanother, and a further lack of adequate monitor-ing to evaluate effectiveness and nontargetimpacts. Moreover, poor coordination of biologi-cal control programs among government agen-cies can result in replication of effort;conversely, the agencies sometimes end upworking at cross purposes (see box 5-2 ).

Better coordination of biological control workwould increase the potential for success andreduce the costs and risks (82). Biological con-trol is worth supporting because of the highpotential payoffs when it succeeds. By coordina-tion, researchers usually mean disseminatinginformation about ongoing work, enabling col-laborative efforts, making research findingsreadily available, and maintaining good data-bases of biological control introductions andtheir results. Good databases are essential todevelop biological control into a more predictivescience (see chapter 3). In addition, goodresearch in biological control requires supportover a period of years, far longer than is the normin most funding cycles. What biological controlworkers seek is a centralized administration thatwould coordinate the various sequential andinterdependent activities required for a biologicalcontrol program, including assistance with satis-fying regulatory requirements. Such coordinationcould incorporate private sector involvement inthe production and dissemination of natural ene-mies (see chapter 6 options). It might also deal

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with use of biological control in non-agriculturalhabitats, such as in wilderness preserves andaquatic ecosystems. The coordinating mecha-nism might range from an organization that sim-ply coordinates information and needs to a singleentity responsible for all aspects of biologicalcontrol research and implementation.

The harshest critics say that the necessarycoordination is virtually nonexistent today (58).In fact, two USDA entities, the National Biologi-cal Control Institute (in APHIS) and the Inter-agency Biological Control CoordinatingCommittee (IBC3) were designed for this func-tion. Neither fulfills it perfectly—the institutebecause it is located within an operations agencyand lacks funds and authority; the committeebecause it has largely ceased to function.

Representatives of the Agricultural ResearchService suggest that their agency, through itsNational Program Staff, should be the coordinat-ing site (320). However, ARS has not shoulderedthis responsibility under its existing structure,and this option would suffer the same (real orperceived) problem as the National BiologicalControl Institute—it would place responsibili-ties for coordination within a single agency hav-ing its own vested interests.

Congress could select either theNational Biological Control Institute, the InteragencyBiological Control Coordinating Committee, or a newunit (perhaps incorporating both organizations) as theinstitutional site for national coordination of biologicalcontrol. Selection of the National Biological ControlInstitute would require its elevation to a higher levelwithin USDA, because its current position makes itaccountable to the priorities of one agency (APHIS).Selection of the Interagency Biological Control Coor-dinating Committee would require revitalizing the nowinactive committee. Specific coordinating responsibil-ities and appropriations would need to be assigned towhatever organization is selected.

Alternatively, Congress could create acentralized agency responsible for all federal activi-ties related to biological control. This option seemsonly remotely feasible today, because biological con-trol programs are dispersed throughout at least eight

agencies, in many cases related directly to their pestcontrol responsibilities.

Congress could strengthen and stabilizethe new biological control program within the NationalResearch Initiative, and also make provisions so thatCSREES could fund some projects of long durationrather than the five-year grants the agency says aremandated by current law. Note that the NationalResearch Initiative program on biological control hasnot received strong support from the current Con-gress and might be eliminated in fiscal year 1996.

Should Congress choose to fund theUSDA IPM Initiative, it could stipulate that the desig-nated organization for coordinating biological controlbe a participant. Even without designating a coordi-nating organization, Congress could require that theNational Biological Control Institute be involved in theinitiative to help integrate biological control and IPMprograms (see also chapter 3 for discussion of prob-lems related to a lack of coordination between biolog-ical control and IPM).

Congress could direct USDA to maintaina consistent and comprehensive database on biologi-cal control introductions. Several different institutionalsites might be possible. Previous attempts at develop-ing such a database in the Agricultural Research Ser-vice suffered from erratic support. The history of poordocumentation and recordkeeping by the APHIS reg-ulatory unit that permits biological control introduc-tions (see chapter 4) makes it seem an equallyproblematic site at this time; although whatever dataare developed by APHIS via the permitting processshould be incorporated into the biological controldatabase. Other possibilities include the NationalAgricultural Library or the National Germplasm Pro-gram. Development of a biological control databasecould occur even if no coordinating structure for bio-logical control is designated.

❚ Addressing Currently Unmet Research NeedsAlthough this report does not seek generally toaddress details of what specific BBT researchshould be conducted,14 gaps in two areas have

14 In part this is because the upcoming report from the National Research Council should do a thorough analysis of this topic.

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become particularly obvious during the course ofthe assessment. First, examination of the propor-tion of federal funds going to research on variouscategories of pests shows an obvious slanttowards insect pests (figure 5-3), Weeds receivea disproportionately small allocation, eventhough herbicides represent the single greatestcategory of pesticide use in the United States,accounting for approximately 59 percent of pes-ticides used in agriculture and 57 percent of

15 (399). The emphasis onoverall pesticide useinsects may be a historical artifact of when BBTresearch developed, because the widespread useof herbicides is a relatively recent practice inU.S. agriculture. Nevertheless, it means that asignificant category of pests currently receivesrelatively little attention. In the absence of anyaction, this pattern is likely to continue; the exec-utive branch’s budget proposal for fiscal year1996 eliminated funding for the ARS biologicalcontrol of weeds project in California and theArmy Corps of Engineers program for biologicalcontrol of aquatic weeds.

A second major gap is the followup and moni-toring of BBTs, especially biological control.Very little of this type of work is conducted inthe United States. According to biological con-trol workers, such research will be essential todevelop better predictive capabilities and there-fore streamline biological control projects (seechapter 3). The lack of followup has anotherimportant consequence. It makes evaluation ofthe potential nontarget impacts of BBTs excep-tionally difficult to assess, resulting in a regula-tory system based more on assumptions aboutsafety rather than on documentation to that effect(see chapter 4).

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R e s e a r c h S e r v i c e a n d t h e C o o p e r a t i v e S t a t e

Research, Education, and Extension Service to allo-cate a greater proportion of their research fundingtoward control of weeds,

OPTION Congress could direct all federal agen-cies that conduct or fund biological control programs

Nematodes5%

Insects55%

Plant pathog25%

SOURCES: D.M. Gibbons, The EOP Foundation, Inc., Washington,DC, Report on the Role of the USDA in Biologically-Based Pest Con-trol Research, ” unpublished contractor report prepared for the Office

of Technology Assessment, U.S. Congress, Washington, DC, January1995; J.R. Nechols and J.J. Obrycki, Kansas State University and

lowa State University, “OTA Preliminary Assessment of Biological

Control Current Research, ” unpublished contractor report preparedfor the Office of Technology Assessment, U.S. Congress, Washing-

ton, DC, January 1994,

NOTE. EPA, APHIS, and states are not included because research

and development could not be identified by pest type

to initiate or fund monitoring projects, especially forhigher risk categories (see chapter 4 for discussion of

risk categories). One way this might be accomplished

is to give higher priority to research projects that

include a monitoring component.

❚ Maintaining the NecessaryLevel of Technical ExpertiseAt a nationwide scale, technical expertise is lack-ing in certain key areas for the development andimplementation of BBTs. For example, two sig-nificant obstacles to increased use of BBTs arethe lack of adequate incorporation into 1PM pro-grams (see chapter 3) and the paucity of relatedinformation about BBTs available to users. Partof the problem lies with the lack of staff ade-quately trained in BBTs and 1PM within theCooperative Extension System.

15 Percentages calculated according to weight of active ingredient.

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Chapter 5 From Research to Implementation | 143

A second area where adequate expertise is dis-appearing is the field of taxonomy and systemat-ics. The number of qualified taxonomists isshrinking; yet the discovery and development ofnew biological control agents, because of theirspecific nature, relies on accurate taxonomy—the identification and classification of livingorganisms (142,186).16 Funds and resources fortaxonomy and biosystematics are difficult toobtain, and critics say the science is consideredto have relatively low priority among ARSadministrators (58). According to the naturalenemy industry, only one U.S. scientist can iden-tify various species of Trichogramma wasps thatare among the most commonly sold natural ene-mies in the United States. Incorrect identifica-tions can lead to a mismatch of biological controlagents with their pest targets, or to poor controlagents unintentionally being sold as natural ene-mies. Moreover, an accurate and knowledge-richclassification is essential to enable a more pre-dictive approach to biological control (186).

Congress could support education inIPM through the Land Grant University system. Vari-ous approaches might be possible, for example,funding graduate fellowships in IPM.

Congress could direct the AgriculturalResearch Service to increase resources and staffslots allocated to the Biosystematics Laboratory forwork related to biological control.

Postdoctoral fellowships from APHIS’sNational Biological Control Institute have been usedsuccessfully to support U.S. taxonomic work. Con-gress could direct APHIS to allocate a larger share ofits biological control funding for this purpose.

❚ Educating and Influencing UsersA significant weak link in the implementation ofBBTs is getting farmers to experiment with thesetechnologies. Many lack sufficient informationto make informed decisions, and the availabletechnical support may be strongly biased in favor

16 Taxonomy is part of the larger field of biosystematics that examines broad aspects of the relationships among living organisms (speciesand higher taxonomic categories like families).

of conventional approaches. Today, extension’sdirect role in educating farmers about pest con-trol has been dwarfed by that of private consult-ants. Congress could help improve access ofprivate consultants to information on BBTs andIPM in several ways.

The Federal Insecticide, Fungicide, andRodenticide Act prohibits the federal governmentfrom requiring training in IPM for certification of pesti-cide applicators. Congress could amend the act torectify this situation and require that pesticide appli-cators be knowledgeable in the full range of pest con-trol options, including BBTs.

Several different types of consultantsaffect pesticide use decisions. Several professionalassociations influence the types of information theseconsultants provide through training programs andcertification standards. Extension has worked with atleast one society, the Agronomy Society, to help inte-grate IPM into their certification program. Congresscould encourage similar efforts through the Coopera-tive Extension System, perhaps by providing targetedcompetitive funds for projects that involve collabora-tion between extension personnel and professionalsocieties to integrate BBTs and IPM into training pro-grams or certification standards.

Certain financial incentives are thought tosway farmers’ decisions in favor of conventionalpesticide-based methods, such as cosmetic stan-dards. In addition, constraints on the availabilityor cost of conventional pesticides affect the arrayof affordable pest control options available tofarmers. Several agricultural economists havesuggested that markets for BBTs could beexpanded by creating incentives for farmers touse these approaches or disincentives to use con-ventional approaches (e.g., taxing conventionalpesticides).

One problem with this approach is it assumesthe availability of BBTs is directly driven bymarket forces. However, BBT research, espe-cially in certain areas, is primarily publiclyfunded at this time. OTA has found that clear

OPTION

OPTION

OPTION

OPTION

OPTION

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mechanisms have not existed to match thisresearch to the needs of farmers orother users. Policy changes that increase thedemand for BBTs, but neglect to improve thesupply of BBTs coming through the pipeline,

might be a set-up for failure. Adjusting theresearch agenda to better ensure that BBTs makeit into the hands of farmers and other users willbe an important part of policies that seek todecrease pesticide use.

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| 145

6Commercial

Considerations

ndustry involvement in the production ofbiologically based pest control products issomething of a mystery to outsiders. Misin-formation—especially gross under- and

overestimates of the current and potential futuresignificance of the private sector role—abounds.For example, some researchers unrealisticallyexpect that the private sector will pursue everypromising technology, ignoring the fact thatinvestment makes sense only if a companystands to make a profit. At the opposite extreme,others equally incorrectly believe that biologi-cally based pest control should be left entirely tothe public sector—that there is no appropriaterole for the private sector. This view ignores thetremendous vested interest of the private sectorin conventional pesticides, which must be incor-porated into planning for the future of thenation’s pest management practices.

This chapter explores the commercial produc-tion of biologically based pest control products.It identifies the size and structure of the industry,its relationship to the production of conventionalpesticides, industry trends, and the ways that allof these elements influence the extent of futureadoption of biologically based methods. Thechapter concludes by discussing the numerous

direct and indirect influences that the federalgovernment exerts over producers of biologicallybased technologies for pest control (BBTs) prod-ucts and by suggesting ways that the governmentcould encourage commercial activity in this area.

Only certain biologically based technologieslend themselves to commercial production of amarketable product. These include: augmentativereleases of natural enemies; deployment of pher-omone-based traps and mating disrupters; andapplications of microbial pesticides. In contrast,no commercial involvement occurs in classicalbiological control where the agent becomesestablished, reproduces itself, and provides con-tinuing pest control without further intervention(options to contract out production of naturalenemies to commercial insectaries, however, arediscussed later in this chapter). Only governmentagencies thus far have used sterile maleapproaches; some companies that have examinedthe commercial potential of the method haveconcluded that there are significant technicalimpediments. Conservation of natural enemiesthrough cultural practices or choice of pesticidetype also occurs without purchase of any biologi-cally based product (317).

I

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STRUCTURE OF THE BBT INDUSTRYBiologically based products are a small butgrowing part of the pest control industry in theUnited States and worldwide. The market forBBTs is unevenly distributed geographically andalso across pest control sectors. The companiesinvolved range from small owner-operated firmsto large multinational corporations. The products

also are diverse, although various Bt-basedinsecticides account for the majority of sales atpresent.

❚ Market ShareBBTs currently command only minute fractionsof the $6 billion to $7 billion U.S. market and the$24 billion to $25 billion worldwide retail mar-

Chapter 6 Findings

■ Biologically based products now make up about 2 percent of the market for pest control in the United

States and 1 percent or less of the international market, with annual worldwide sales of $180 million to$248 million. These products, however, represent one of the fastest growing sectors of the pest control

industry.

■ Almost all of the biologically based products sold commercially to date have been for control of insectpests. Because only about 29 percent of the conventional pesticide market is aimed at insect control,

however, biologically based technologies for pest control (BBTs) are likely to capture a significant pro-portion of this market in the near term.

■ The industry that produces natural enemies for pest control is small but growing, with annual U.S.

sales estimated at $8 million and worldwide sales at $40 million. The industry faces substantial hurdlesto expanded sales. Some reflect technical aspects of product development, manufacture, quality con-

trol, and distribution. Others occur because natural enemies do not fit easily into conventional pestcontrol systems or measure up to farmers’ expectations for product efficacy based on their experience

with conventional pesticides.

■ Venture capital is the foundation of the midsize biotechnology companies that have been the nation’slaboratories for the discovery of new microbial pesticides. Because companies have been slow to real-

ize profits from biologically based pest control products, their future is somewhat uncertain. The finan-cial instability has contributed to numerous mergers and acquisitions or agreements with larger

agrochemical companies.

■ The conventional pesticide industry has shown some interest in biologically based pest control prod-ucts, with even the largest companies like Ciba-Geigy developing related product lines. Overall invest-

ment for research in this area, however, remains only a small fraction of that devoted to conventionalpesticides. Big agrochemical and pharmaceutical companies seek products with large markets and

sizable returns on investment—criteria satisfied by none of the BBTs now sold commercially. Somebelieve that genetically engineered microbes hold the greatest promise. The big companies are

poised to acquire smaller biotechnology and natural enemy companies if technical breakthroughs orother factors should result in significant market growth for BBTs.

■ Today’s pesticide industry has developed around the research, development, and marketing of con-

ventional pesticides, and biologically based products do not move smoothly through this structure.Various other factors, some having little relationship to federal policies or programs, also will influence

the commercial future of BBTs. Development of favorable federal policies could enhance R&D of BBTproducts and speed up growth of their markets, but even under the most favorable conditions, biolog-

ically based products will not replace a significant proportion of conventional pesticides over the next10 to 15 years.

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Chapter 6 Commercial Considerations | 147

ket for crop protection (table 6-1). The availableestimates of market share for BBTs are impreciseand probably err on the side of optimism. Never-theless, even the most conservative analysts pre-dict that the market for BBTs will grow morerapidly than the market for conventional pesti-cides which is expected to expand only 2.5 to 3percent annually over the next five years(149,150). Estimated annual growth rates for glo-bal sales of BBTs in general and for each majorcategory of BBTs in particular (natural enemies,pheromones, microbial pesticides) range from 5to 30 percent, with most predictions around 10percent (301,14,150,294,413).

Almost all sales to date have been of productsto control insect pests (figure 6-1) (149). Accord-ing to some sources, Bt-based productsaccounted for more than 90 percent of worldwidemicrobial pesticide sales in 1990 (294). All pher-omone-based products and most natural enemyproducts currently on the market are for controlof insect pests. BBTs now account for 2.5 to 3.5percent of worldwide insecticide sales. Some

experts predict that growth of BBT sales in theimmediate future will be unevenly distributedacross the pest control market, occurring prima-rily in the insect control sector where productR&D and a track record of field efficacy are bestestablished for Bt (149). Others assert that the Btmarket has reached a plateau and that futuregrowth will result from types of products basedon viruses and fungi (e.g., the use of fungi tocontrol household pests like termites and cock-roaches) (233).

The geographic distribution of BBT sales alsois uneven. North America and Europe accountedfor approximately 60 percent of the total Bt mar-ket in 1991 (287). The United States accountedfor an estimated 55 percent of all worldwidesales of microbial pesticides and natural enemies(294). The Far East represents a potentially sig-nificant but poorly understood market of about$47 million annually (287,149). While naturalenemy sales occur primarily in North Americaand Europe, augmentative uses in developing

TABLE 6-1: Estimated Market Value of Biologically Based Pest Control Products (millions of dollars annually: 1990, 1991, or 1992)

Natural enemies Pheromonesa Microbial pesticides All BBTs % Total marketb

United States $8 $30 to $42 $56.7 to $97 $94.7 to $147 1.3% to 2.4%

Worldwide $40 $60 $104.5 to $147.5 $180 to $247.5 0.7% to 1.0%

a Pheromones may include some products for pest monitoring as well as control. Sources do not report the data in a way that would allow thislevel of discrimination.b Percentage of total worldwide market for pest control products based on an estimated total retail market of $24 to $25.2 billion.

SOURCES: Compiled from M.G. Banfield, An Analysis of the Semiochemical Industry in North America, 1991; J. Houghton, Houghton and Asso-ciates, St. Louis, MO, “The View of Biological Pest Control From the Pesticide Industry,” unpublished contractor report prepared for the Office ofTechnology Assessment, U.S. Congress, Washington, DC, 1993; J. Houghton, “Biologically-Based Technologies For Pest Control: Workshop onthe Role of the Private Sector,” unpublished contractor report prepared for the Office of Technology Assessment, U.S. Congress, Washington,DC, September 20–21, 1994; P.B. Rodgers, “Potential of Biopesticides in Agriculture,” Pesticide Science, 39(2): 117–129, 1993; “Sales of Biope-sticides Expected to Rise at the Expense of Chemically-Based Pesticides,” Pesticide Outlook, 4–5, February 1994; K.R. Smith, Henry A. WallaceInstitute for Alternative Agriculture, Hyattsville, MD, “Biological Pest Control: An Assessment of Current Markets and Market Potential,” unpub-lished contractor report prepared for the Office of Technology Assessment, U.S. Congress, Washington, DC, January 1994; G. Voss and B. Mif-lin, “Biocontrol in Plant Protection: CIBA's Approach,” Pesticide Outlook 29–34, April 1994.

NOTE: Numbers presented are composites of annual data for 1990, 1991, or 1992 and show the full range of estimated values obtained by OTA.Estimated market values for biologically based pest control products are difficult to obtain, vary greatly with the source, and should be viewedwith skepticism. Those involved in the developing or producing of biologically based pest control products tend to provide optimistic numbers.The most widely cited estimates come from consulting firms that summarize market trends and then sell their analyses to the private sector.Accuracy of these analyses is difficult to judge because the sources and data are proprietary. Despite the inexactitude, experts agree that therelative magnitudes of commonly reported numbers are correct.

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148 Biologically Based Technologies for Pest Control

100

80

60

40

20

0Control of weeds Control of insects Control of plant

and nematodes pathogens

based products a

SOURCES: Office of Technology Assessment, 1995; (data on pesti-

cide sales) A. Aspelin, “Pesticide Industry Sales and Usage: 1992

and 1993 Market Estimates, ” U.S. Environmental Protection Agency,EPA Report No. 733-K-94-001 (Washington, DC: June 1994).aLevels for BBTs estimated by OTA based on known product types

and relative sales,

countries like Colombia and China are thought tobe high but traditionally supplied by governmentrather than sources in the private sector. How-ever, South and Central America have witnessedrapid movement toward privatization of theindustry within the past three to five years; some7 to 10 percent of the natural enemies producedin the United States are sold in Latin America(28). The Japanese government has also taken anoncommercial approach to control of Fusariumwilts (plant diseases) by distributing a microbialcontrol agent (22).

Most sales of BBT are to users in agricultureand forestry; only a small fraction of sales are forgardening and other uses (317). Major arablecrops like corn and cotton account for only asmall proportion of the market (e.g., 7 percent ofthe Bt market in 1992) (294).

❚ Companies and ProductsCompanies that produce biologically based pestcontrol products have total annual sales thatrange from less than $50,000 to billions of dol-lars (including non-BBT product lines). Thecompanies roughly break down into those mar-keting natural enemies, those marketing phero-mone-based products, and those marketingmicrobial pesticides. However, the growing fre-quency of various acquisitions, partnerships, andagreements among companies increasingly blursthese distinctions. A few of the largest compa-nies have entered markets for all types of prod-ucts.

Natural EnemiesAs many as 132 companies in North Americaproduce or supply natural enemies (155);approximately 25 to 30 of these companies arecommercial insectaries (37). A relatively fewlarge companies dominate worldwide produc-tion. The two largest are Koppert, B. V., in theNetherlands which has annual revenues of about$20 million and distributors in more than 20countries, and Bunting and Sons in Great Britain(317). Ciba-Geigy, the world’s largest producerof agrochemicals, bought Bunting in 1993 (413).About half of all natural enemy companies arelocated in North America, where most are smalland family operated. Only about a half-dozenU.S. companies have annual sales exceeding $1million. Although the total number of NorthAmerican companies is small, it is large relativeto current market demand, and thus competitionis intense (317).

The Association of Natural Bio-Control Pro-ducers (ANBP), founded in 1990, is a trade asso-ciation of about 100 members representing theinterests of North American natural enemy com-panies. Some 22 of the members of this organiza-tion are commercial producers, representingapproximately 85 percent of North Americancommercial insectaries and more than 90 percentof the North American wholesale market of natu-ral enemies (317). But only one-fifth of theroughly 100 distributors of natural enemies in

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Chapter 6 Commercial Considerations | 149

North America belong to ANBP (37). The Inter-national Organization of Biological Control(IOBC) is an active and long-standing interna-tional association that represents the industry aswell as others engaged in researching or imple-menting biological control programs (317).

Natural enemy products marketed worldwideconsist of more than 100 species, primarily ofinsects and mites that prey upon or parasitizepests (317). In addition, a handful of companiessupply snails or vertebrate animals, such as themosquito fish, Gambusia affinis, for biologicalcontrol. The most widely used natural enemiesare various species of the wasp Trichogrammathat parasitize caterpillar pests (317). No industryanalyses compile data on production or salesaccording to type of product (317). Box 6-1 lists

the products that appear to be marketed most fre-quently.

Sales of natural enemies in the United Statesreportedly grew rapidly over the past five years(28), but significant hurdles to expansion exist.These are related to the nature of natural enemyproducts, production methods, and the industry’sstage of development.

Natural enemies are shipped as live eggs, lar-vae, or adults. These living products have a shortshelf life and require attentive (temperature-con-trolled) handling. Applications in the field mustbe carefully timed according to weather, pestabundance, and pesticide spray schedules. Cur-rent production techniques are hands-on, laborintensive, and expensive because natural enemies

BOX 6-1: Biologically Based Products for Pest Control

Types of natural enemies sold most frequently

Lacewings (Chrysoperla carnea, Chrysoperla rufilabris)

■ Primarily for aphid control, but also for mealybugs, thrips, scales, and various other insects in fields

or glasshouses

The parasitic wasp Encarsia formosa

■ For control of whitefly

Various species of parasitic wasps in the genus Trichogramma

■ For control of caterpillar pests such as European corn borers, corn earworms, boll worms, bud-worms, armyworms, and hornworms

Predatory lady beetles (primarily Hippodamia convergens and Cryptolaemus montrouzieri)

Various predacious and parasitic mites

■ Primarily for control of thrips in glasshouses and spider mites

The aphid gall midge (Aphidoletes aphidimyza)

■ For control of aphids in glasshouses

Pheromone products currently marketed or under d evelopment

For Disruption of Pest Mating:

■ Products targeting 16 different insect pests

Lure and Kill (pheromone and insecticide combinations):

■ 10 different products targeting five different insect pests

Microbial pesticides currently sold commercially

For Insect Control:

■ Bt (Bacillus thuringiensis), at least eight different varieties of bacteria marketed under more than 17different trade names

■ One genetically engineered Bt product

(continued)

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are reared on live hosts (commonly referred to asin vivo production).

Great interest centers on the development ofbetter production, packaging, storage, shipping,application, and quality control techniques toreduce cost, enhance shelf life, and improveproduct efficacy (317). Industry analysts say thatsuch improved production and handling wouldgreatly decrease the cost of using natural ene-mies (table 6-2). Another lesser interest of theindustry is improvement of breeding stock toenhance compatibility with conventional pesti-cides. Some companies already do this by select-ing stock from regions where pesticide use ishigh, and academic researchers have begunexperiments to select or to genetically engineercertain natural enemies (mites) for herbicideresistance.

Because most natural enemy companies aresmall and operate with a low profit margin, fewcan afford to invest significantly in R&D (317).The industry would like to see far greater publicinvestment in research, for example, to developartificial diets for rearing natural enemies (invitro production). They assert that the currentrelationship between the industry and the USDAAgricultural Research Service (ARS) has muchroom for improvement (34). Much of the ground-work for commercial production of natural ene-mies was laid by past federal research thatdeveloped production techniques and identifiedpotential biological control agents. Producerscomplain that this technology transfer pipelinebegan drying up some time ago and has hardlyexisted at all for the past six to seven years (270).

■ Three genetically engineered products consisting of Bt toxin genes inserted into a killedPseudomonas fluorescens

■ Bacterial milky spore disease of the Japanese beetle (Bacillus popolliae, B. lentimorbus)

■ One fungal pathogen for cockroach control (Metarhizium anisopliae)

■ Two fungal products for control of turf and ornamental pests (Beauvaria bassiana)

■ Two viruses (gypsy moth NPV and beet armyworm NPV)

■ A protozoan pathogen of grasshoppers (Nosema locustae)

■ Four nematode species in the families Steinermatidae and Heterorhabditidae

For Weed Control:

■ Two fungi that cause plant disease (both were taken off the market, but one has recently been rein-troduced; see chapter 3)

For Control of Plant Diseases:

■ Eight microbial antagonists of plant diseases, including: Gliocladium virens for use in soiless plant-ing mixtures; Trichoderma harzianum for use in potting mixtures and as a golf course inoculant;

Agrobacterium radiobacter for control of crown gall: Bacillus subtilis for seed treatment; Candidaoleophila and Pseudomonas syringae for control of postharvest plant disease

SOURCES: J.O. Becker and F.J. Schwinn, “Control of Soil-Bourne Pathogens with Living Bacteria and Fungi: Status and Outlook,”Pesticide Science 37:355-363, 1993; B. Cibulsky, Manager, Licensing and Business Development, Abbott Laboratories, letter tothe Office of Technology Assessment, U.S. Congress, Washington, DC, August 18, 1995; G.E. Harman and C.K. Hayes, CornellUniversity, Geneva, NY, “Biologically-Based Technologies for Pest Control: Pathogens that are Pests of Agriculture,” unpublishedcontractor report prepared for the Office of Technology Assessment, U.S. Congress, Washington, DC, October, 1994; K. Smith,Henry A. Wallace Institute for Alternative Agriculture, Greenbelt, MD, “Biological Control: An Assessment of Current Markets &Market Potentials,” unpublished contractor report prepared for the Office of Technology Assessment, U.S. Congress, Washing-ton, DC, January 1994; and R.G. Van Driesche et al., University of Massachusetts, Amherst, MA, “Report on Biological Control ofInvertebrate Pests of Forestry and Agriculture,” unpublished contractor report prepared for the Office of Technology Assessment,U.S. Congress, Washington, DC, December, 1994.

NOTE: Table primarily reflects products marketed in the United States.

BOX 6-1: Biologically Based Products for Pest Control (Cont’d.)

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Chapter 6 Commercial Considerations | 151

Although improved products and productionmethods might help natural enemies competemore effectively against other pest control prod-ucts in the marketplace, other obstacles remain.Most important, natural enemies are highly spe-cific, and suppress but do not locally eliminate apest. Their performance profile differs signifi-cantly from that of conventional pesticides (seechapter 3). Industry representatives believe thatbetter education of farmers—through extensionpersonnel and pest control advisors with specifictraining in BBTs—will be essential for the devel-opment of larger markets (see chapter 5).

Perhaps equally important, the effectivenessof commercially available natural enemies underfield conditions remains hotly debated, withsome academic scientists claiming that the prod-ucts have little utility except in glasshouse horti-culture. The sources of differing views oneffectiveness are difficult to untangle. There istoo little information about how natural enemiesshould be applied to maximize their impact onpests (i.e., when, where, how, and how many peracre). Nor has the effectiveness of most naturalenemies—and the extent to which that effective-ness is affected by care in product handling anduse—been adequately evaluated (12).

Some scientists believe that the quality controlof natural enemy products fluctuates widelyamong producers, although adequate documenta-tion of this problem is lacking. Instructions onappropriate application rates also vary greatly

among companies (59A). Some companies fearthat poor products with improper use will destroythe industry’s public image (285). The industryhas been moving toward voluntary quality con-trol standards through activities of the ANBP inthe United States and of the IOBC internationally(12,157). Companies fear that the federal gov-ernment will move to regulate the industry ifthey do not institute such voluntary controls.

The USDA Animal and Plant Health Inspec-tion Service (APHIS) recently published draftregulations for the importation, interstate transit,and use of biological control agents1 (see chapter4). These regulations, which would have put sig-nificant new requirements in place, were with-drawn following negative public comment.Natural enemy producers now consider futurefederal regulation of their industry to be amongtheir greatest challenges and wish to participatein the development of any new rules.

Finally, the market for natural enemies ishighly volatile (317), fluctuating with productionlevels of those crops for which natural enemiesare most commonly deployed. The market alsodepends on pest abundance, which, in turn, isgreatly affected by the weather and other envi-ronmental variables. These problems woulddiminish if markets and types of crops servicedincreased. For now, though, producers have greatdifficulty predicting the market for certain prod-ucts and increasingly are turning to narrowerproduct lines that have more consistent sales.

1 Federal Register 60(116):31647, June 16, 1995.

TABLE 6-2: Projection: How Improved Production and Handling Technologies Would Incrementally Increase the Scale and Decrease the Costs of Trichogramma Production

ImprovementIncrease in production capacity

(hectare per season)Reduction in cost

per hectare

University R&D — —

Industrial pilot plant (to scale-up production techniques) × 15 50% reduction

Longer shelf life × 5 No change

Improved techniques for field application × 24 96% reduction

Artificial diets × 22 88% reduction

Total change with all improvements × 40,000 99.8% reduction

SOURCE: Adapted from G. Voss and B. Miflin, “Biocontrol in Plant Protection: CIBA's Approach,” Pesticide Outlook 29–34, April 1994.

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Although this move reduces the companies’ eco-nomic exposure, it provides fewer options forfarmers and other users to experiment with natu-ral enemies for suppressing a variety of pests.

PheromonesPheromone-based insect traps or mating disrupt-ers are produced by 14 North American compa-nies, including Ecogen, Consep Membranes,Hercon Environmental, and Troy Biosciences.Only two or three companies in the United Statesactually synthesize the pheromones used in pher-omone-based products. These chemicals are thenincorporated into dispensers and traps by thecompanies marketing those products.

Producers of semiochemicals2 bandedtogether in 1992 to form the American Semio-chemicals Association (ASA). In part as a resultof the association’s efforts, the U.S. Environ-mental Protection Agency (EPA) moved to relaxregulatory oversight of pheromone registrationand sales in 1994, and the industry seems to havefew complaints about the federal regulatory sys-tem currently in place.

Pheromone products include devices for mon-itoring pest populations, mass trapping ofinsects, mating disruption, and bait-and-kill com-binations also containing a conventional pesti-cide or viral or fungal based pesticides. Matingdisruption products have been developed forsuch well-known pests as the pink bollworm(Pectinophora gossypiella), Oriental fruitmoth(Grapholita molesta), and tomato pinworm(Keiferia lycopersicella). Current bait-and-killproducts target the American cockroach(Periplaneta americana), and the boll weevil(Anthonomus grandis).

Pheromone products can be easily incorpo-rated into current pest management practicesbecause they are compatible with any pesticidespray schedule. For example, pheromones arenow used widely in the western United States to

2 Semiochemicals refers more generally to naturally occurring chemicals that mediate behavior between living organisms. Pheromonesare a type of semiochemical.

disrupt mating by the codling moth (Cydiapomonella) in apple and pear orchards (259).They also play an integral part in integrated pestmanagement (IPM) systems as tools for monitor-ing pest abundance.

Like natural enemies, pheromones used forsuppressing pests are highly target specific andgenerally reduce, but do not locally eliminate,pests. Some have proven very effective at sup-pressing pests of high densities, however (39).Moreover, they are “adult-based” strategies andare most effective when deployed in concert withother pest control tools that attack larvae as well.The need to use pheromones as one of severalcomponents in a pest control system can confusefarmers more accustomed to “stand alone” pesti-cide products, leading to failures in the field anda lack of confidence in pheromone-basedapproaches.

Pheromone products vary in the amount andtype of information included to instruct the useron proper use—for example, whether theyaddress product strength, recommended han-dling, or expiration.3 Research scientists worrythat such inconsistent instructions can furtherundermine consumer confidence by contributingto incorrect use and poor performance. The Ento-mological Society of America (ESA), an organi-zation of professional entomologists fromacademia, industry, and government, is workingon a paper recommending that the industry adoptvoluntary standards for including this type ofinformation on the labels of monitoring products(87). Some industry representatives, however,question the need for such standards, arguing thatpoorly performing products will eventually beeliminated through diminished sales. In addition,some of the technical information that scientistswould like to see displayed is proprietary infor-mation for the companies.

The federal research system historically was asignificant source of new information on phero-

3 Such information would be in addition to the standard data required by EPA for labels of pest control products. No federal labelingrequirements exist for pheromone products intended for monitoring pests.

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Chapter 6 Commercial Considerations 153

mones. Industry representatives complain thatthe level of federal research in this area hasdeclined substantially over the past 10 to 15years, and that federal researchers have conse-quently ceased to provide enough new discover-ies of potential commercial merit (126). The costof such research is too high for the companies toshoulder on their own (116). The specific area inwhich federal scientists could now make the big-gest contribution is in evaluating the field perfor-mance of formulations (persistence and rate ofpheromone release) (39,1 16).

The Federal Technology Transfer Act of 1986permits federal scientists to patent their discover-ies and sell limited licenses for their use. Thislegislation has had mixed results. Whereas thelicensing process has provided incentives forcooperation between federal researchers andindustry, some discoveries have been lost whenthey have been licensed to companies that cannotor do not develop the product (126). In addition,some smaller companies have difficulty meetingthe financial requirements for obtaining licensesfor the products of federal research.

The gap in the discovery and development ofnew products also means that the industry is nowcrowded by a large number of companies com-peting for a small number of product types anduses (23). Industry representatives predict theultimate result to be a reduction in the number ofcompanies involved because of company merg-ers, acquisitions, and failures (23). This processis already under way; a number of pheromonecompanies have recently been purchased by agri-cultural biotechnology companies, for example,Agrisense by Biosys (136). Some pheromoneproducers worry that this consolidation may ulti-mately destabilize the industry because many ofthe biotechnology companies are not themselvesin sound financial condition. The situation inEurope-where a number of large companies,like BASF, are involved in developing phero-mone products-offers an interesting contrast.There, strong government policies to reduce theuse of conventional pesticides have stimulatedthe involvement of larger companies (39).

Microbial PesticidesMore than 20 companies develop or producemicrobial pesticides worldwide (317). A few aresmall companies that market only one or a fewproducts with annual sales of less than $1 mil-lion. Some are midsize biotechnology companieslike Biosys, Ecogen, and EcoScience, which pro-duce a diverse mix of products. Numerous largeragrochemical and pharmaceutical companies,like Ciba-Geigy, Abbott Laboratories, and San-doz also are involved. For these, microbial pesti-cides account only for a fraction of annual sales(317). The interest of the pharmaceutical compa-nies has been driven by their easy access to thelarge-scale fermentation equipment necessary forproduction of microbial pesticides (150).

Most U.S. producers of microbial pesticidesare members of the Washington-based Biotech-nology Industry Organization (BIO). This tradeassociation serves as both a lobbyist and a sourceof educational seminars for members of the bio-technology industry. In addition, BIO holds con-ferences five times a year where industryrepresentatives gather to discuss the latest tech-nologies and future directions for the industry(333).

Microbial pesticides are formulations of bac-teria, fungi, nematodes, protozoa, or viruses for

Several new microbial pesticides based on fungi, Iike this Beau-veria bassiana on whiteflies, have just become commerciallyavailable.

Agricultural Research Service, USDA

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pest control. Although researchers have exploreda large number of species from more than 20 tax-onomic families of plant or animal pathogen forpotential commercialization, far fewer speciesare available for commercial sale (box 6-1 pre-sented earlier) (317). A total of 43 strains/speciesand 245 products are now registered with theEnvironmental Protection Agency (396). Theindustry’s greatest focus, by far, has been on theidentification and development of strains of thebacterium Bacillus thuringiensis (Bt) which con-tain insect toxins. As many as 40,000 differentstrains have been identified and archived.

Microbial pesticides may have achieved thegreatest market share of BBTs today because Btis easy to use and compatible with conventionalpesticides. Farmers use the same equipment andmethods to apply Bt-based products and conven-tional pesticides, and thus do not require substan-tial retraining to use them (317). Consequently,farmers’ acceptance of Bt has been relativelyhigh. An exception is fresh-produce farmers;some believe that use of Bt results in fruits with alower quality appearance (99).

Other microbial pesticides vary in ease of useand compatibility with conventional chemicals.For example, unlike most fungal agents, mostbacterial agents for plant pathogen control arecompatible with fungicides (22). When OceanSpray Cranberries personnel sought to use nema-tode products to control insect larvae in cran-berry bogs, they had to work closely with theproducer to adapt the nematode for applicationbecause the standard methods were too difficult(67).

According to industry analysts, the market formicrobial pesticides today remains modestlargely because of inherent deficiencies in theproducts. Most microbial pesticides have a shortshelf life. Bt, for example, has a shelf life rangingfrom six months to two years, compared with ashelf life of two to four years for conventionalpesticides (211). They also have a short field per-sistence, a narrow spectrum of activity, and aslow rate of action relative to conventional pesti-cides (150). An exception here may be some ofthe new seed treatments coming onto the market

to control plant pathogens. These provide alonger period of control than similar chemicaltreatments (138A).

Some industry representatives believe that thegreatest opportunities for microbial pesticideswill result from genetic engineering to correctthese flaws. Field tests of microbial pesticidescreated by genetic engineering have begun, andfour products are currently on the market: Eco-gen’s Raven and Mycogen’s M-trak, MVP andM-Peril. Genetically engineered microbes havethe additional advantage of being clearly patent-able. Whether naturally occurring strains are pat-entable is more ambiguous; the ability to obtain apatent depends on whether the strain has uniqueand novel qualities, such as the capability of pro-ducing a different protein or killing a differentkind of insect (250).

Whether genetic engineering will provide aquick route to cheap, highly efficacious, micro-bial pesticides remains to be seen. Because R&Dand registration costs are higher for geneticallyengineered microbes than for naturally occurringones, genetically engineered products must betargeted at bigger markets to recover the R&Dcosts. But competition from conventional pesti-cides is likely to be most intense in those biggermarkets. Moreover, the regulatory environmentis ambiguous, and future public acceptance ofcommercial use is uncertain. Some of the verycharacteristics most desirable to engineer into amicrobial pesticide—increased breadth of activ-ity, faster kill rate, longer field persistence—arethose most likely to generate greater ecologicalrisks (see chapter 4).

In any case, expanded use of microbial pesti-cides will depend on their providing cost-effec-tive pest control. Currently, the cost of usingthese products is relatively high. Companieshave had difficulty achieving economies of scaleby expanding production. Nevertheless, accord-ing to some estimates, biopesticide use costs arefalling. For example, from 1990 to 1993, the costof using Bt to control Colorado potato beetle(Leptinotarsa decemlineata) in the United Statesreportedly dropped from $20 to $10 per acre(294). And Bt products currently used for forest

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insect control are comparably priced to conven-tional pesticides registered for this use (49).

Economic factors may play the greatest role indetermining the future of microbial pesticides.Biotechnology companies have been laboratoriesfor the discovery of diverse microbes with com-mercial potential, and venture capital has beentheir foundation. However, most of the biotech-nology companies have yet to make any profitfrom their products. Some have had difficultybreaking into the Bt market because of theintense competition and domination of largercompanies like Abbott. Even the biggest andbest-known biotechnology companies, like Eco-gen and EcoScience, require continuous capitalinput to stay afloat. The venture capital is begin-ning to dry up, creating some volatility in theindustry and a pullback from R&D investment.In the past 10 years, venture capitalists havedeveloped a negative view of the agriculturalbiotechnology industry because it has spent largeamounts of money on research with very littlereturn. Few venture capitalists now fund biotech-nology, except in the area of medicine (211). Theresult is a series of mergers and consolidations,such as the recently announced purchase of CropGenetics International by Biosys (53).

A number of biotechnology companies havealso formed alliances with larger agrochemicalcompanies (150). Through these, the larger com-pany may provide R&D funding in exchange formarketing rights and thereby gain entry to BBTswithout the expense, time, and long-term com-mitment required to develop an in-house pro-gram. The biotechnology company, in return,may obtain much-needed cash and perhaps assis-tance with formulation, manufacturing, market-ing, or other areas in which the company lacksexpertise.

The shortage of people with the appropriatetraining in production and formulation engineer-ing is one of the factors that make such anarrangement desirable. Industry members believethat this problem needs to be tackled by universi-ties. Some are already doing so; for example, the

University of California at Davis has just starteda new area of study in fermentation engineering,an integral technology in the production ofmicrobial pesticides (211).

VIEW FROM THE CONVENTIONAL PESTICIDE INDUSTRYThe conventional pesticide industry has anambivalent view of biologically based pest con-trol. Most major agrochemical companies haveinvested to some degree in BBTs, but thisinvolvement generally is small and somewhattentative. The ambivalence derives from severalsources, including the companies’ perceptions ofthe positive and negative attributes of biologi-cally based products as well as the larger forcesat play within the pesticide industry.

❚ Participation by Agrochemical CompaniesThe top 10 companies within the agrochemicalindustry are responsible for approximately 72percent of worldwide agrochemical sales (150).All of these companies have supported R&D ofbiologically based pest control products over thepast decade through either internal programs orrelationships with smaller biotechnology compa-nies (150). Worldwide R&D investment by theindustry is estimated at $2.6 billion annually,with approximately $100 million of this allo-cated to BBTs (149). Although agrochemicalcompanies typically put only a fraction of theR&D money into BBTs, this amount is large rel-ative to the R&D budget of midsize biotechnol-ogy companies (233).

A number of the top companies currently mar-ket biologically based products (table 6-3).Despite their dominance of the pest control mar-ket, agrochemical companies do not account forthe lion’s share of worldwide BBT sales. Forexample, about 70 percent of global Bt sales areattributable to Abbott Laboratories and NovoNordisk,4 producers primarily of pharmaceuti-cals and industrial enzymes (150,423).

4 In 1995, Novo Nordisk began to sell its microbial pesticide division.

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Sandoz, ranked about number 12 in globalsales of crop protection products, is the agro-chemical company that is most closely associ-ated with biologically based pest control both inthe United States and worldwide (423). Sandozhas almost 25 years experience in this area. San-doz currently markets pheromone-based prod-ucts and microbial pesticides; it holds anestimated 25 percent of the global market in thelatter (150).

The more recent movement of Ciba-Geigyinto BBTs provoked considerable interestbecause of the company’s status as the world’slargest agrochemical producer (its sales of globalcrop protection products in 1991 were about$12.2 billion) (150). Ciba produces a Bt productand a pheromone product. It entered an agree-ment with Biosys to market that company’s nem-

atode-based biopesticides for turf andornamental applications in 1992 (413). The U.S.component of that agreement was terminated in1995 (79). As mentioned earlier, Ciba-Geigybought Bunting and Sons, one of the world’slargest producers of natural enemies, in 1993.The natural enemy company has not yet beenintegrated with Ciba’s other crop protectionunits. Ciba attempted another entry into produc-tion of natural enemies in 1989 through a jointventure with the government of Ontario todevelop a rearing facility for Trichogrammawasps to control spruce budworm (Choristo-neura fumiferana). However, the company soldits interests in the project in 1994 because itdecided the venture was unlikely to provide asufficient return to justify further funding (413).

TABLE 6-3: Examples of Biologically Based ProductsMarketed by Major Agrochemical Companies or Their Partners

Company Product Description

Ciba Geigy Agree Bt aizawai and Bt kurstaki in a combined formulation for vegetable, fruit, corn, soybean, and tobacco uses

Design Bt aizawai formulation for cotton and soybean uses

Through Ciba Bunting Ltd. markets:

12 natural enemies (including mites) e.g., Trichogramma brassicae wasps, Encarsia formosa, Phyoseiulus persimilis for fruit, vegetable, and ornamental uses

Bunting Steinernema feltiae Nematode formulation for ornamental uses

Bunting Steinernema carpocapsae Nematode formulation for fruit and ornamental uses

Bunting Heterorhabditis megidis Nematode formulation for ornamental uses

Bunting Bacillus thuringiensis Bt formulation for vegetable and ornamental uses

Sandoz Javelin WG Bt kurstaki formulation for vegetable, fruit, and field crop uses

Thuricide Bt kurstaki formulation for ornamental, shade tree, and forest uses

Vault WP Bt kurstaki formulation for vegetable, fruit, and field crop uses

Teknar Bt israelenis for mosquito larvae control

Dupont by agreement markets:

Novo Nordisk's Biobit Bt kurstaki formulation

Crop Genetics International Gypcheck NPV virus formulation for forestry uses produced on contract for the U.S. Forest Service

SOURCE: Office of Technology Assessment, U.S. Congress, 1995.

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❚ Industry Perceptions about Biologically Based ProductsBBTs appeal to agrochemical companiesbecause of the lower costs of bringing such prod-ucts to market, swifter and cheaper registration,apparent environmental safety, and positive pub-lic relations value (150). Recent efforts by theEPA to streamline and speed registration of low-risk pest control products have resulted inreduced data requirements and quicker process-ing of registration applications for BBTs. Bring-ing a microbial pesticide to market now takesroughly three years and costs an estimated $1million to $2 million, in comparison with eight to10 years and $25 million to $80 million for anagrochemical. Costs of meeting registrationrequirements of $20 million for the agrochemicalversus $200,000 for the microbial pesticide con-tribute significantly to the differential, as do therising costs of new agrochemical discovery(294,317).

BBTs generally do not fare well when held upto the performance standards set by conventionalpesticides, however (table 6-4). Most biologi-cally based products generally are effectiveagainst only a few pests, whereas many chemi-cals are “broad spectrum”—providing simulta-neous control of a wider pest array.Environmental conditions and methods of appli-cation can affect the efficacy of some biologicalproducts. Finally, many BBTs have shorter shelflives and field persistence than most conven-tional pesticides. Agrochemical companiesbelieve that farmers are accustomed to the easeof use and effectiveness of conventional pesti-cides and will be reluctant to try biologicallybased products if they cannot offer similar quali-ties (149,150).

Industry expectations for returns on new prod-ucts have been set by conventional pesticides:revenue from a single product can reach $100million annually in the largest markets (e.g.,corn, soybean, wheat, and cotton) (150). Currentbiologically based products cannot compete inthis arena; with the possible exception of Bt,their typical markets are minute in comparison.

Some agrochemical companies believe thatmicrobial pesticides genetically engineered forenhanced efficacy, broader spectrum effects, orlonger field persistence might attain marketsrivaling those of conventional pesticides(149,317). Such companies concentrate whatR&D resources they allocate to BBTs on geneticengineering, anticipating greater returns over thelong term than would be possible by investmentinto the types of BBTs on the market today.

Biologically based products do not fit easilyinto the extensive entrenched system for pesti-cide distribution, sale, and use (149). Conse-quently, even some products that are technicalsuccesses end up being failures in the market-place. Pesticide sales representatives who areunfamiliar with BBTs do not adequately promotethem, and users who have insufficient informa-tion about these products are hesitant to try them.This situation poses special problems because,according to industry representatives, somegrowers rely on sales representatives for advicemore than on extension personnel (149).

Paradoxically, certain especially effectiveBBTs have proved to be commercial failuresbecause they do not have the necessary charac-teristics for success. DeVine, a fungus formula-tion for weed control produced by AbbottLaboratories, provided such good control of itstarget pest that repeated applications were unnec-essary. It could not sustain a large enough marketto justify the company’s production and salescosts, and the product was eventually withdrawnfrom the market. The product was brought backonto the market in 1995 through support of EPA(49).

❚ Other Influences on the IndustryA number of well-performing, low-priced prod-ucts dominate the relatively stagnant market forconventional pesticides (413). Market growth isslow, and profitability declined from 1980 to1991 (150). New products have not been forth-coming despite significant growth in the indus-try’s total R&D; major pesticide manufacturersspent an estimated $1.4 billion on research into

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new products in 1992, up 88 percent from sixyears earlier (294). Few newly discovered chem-istries have matched the desired levels of envi-ronmental and toxicological safety (150). Also,between 1973 and 1993, rates of discovery ofnew agrochemical molecules dropped from onein 5,000 to one in 20,000 (294).

In this context, the rapid market growth and“green” aspects of BBTs have appeal. However,the declining profitability within the agrochemi-cal industry has generated a trend toward consol-idation of companies, and these typically targetnew products at the largest major-use markets,5

5 Major use refers to larger pesticide markets (e.g., those serving corn or wheat).

TABLE 6-4: Comparison of Biologically Based Products and Conventional Pesticides

Natural enemies Pheromones Microbial pesticides Conventional pesticides

Shelf life Short (hours to days)a Moderate (1 to 2 years)

Short to moderate (months)b

Long (years)

Field persistence Shortc Short to moderate (days to weeks)

Short (less than one week)d

Variable (days to years)

Spectrum of activity Narrowe (one pest per product)

Narrow (one pest per product)

Narrow to moderatef (one to several pests per product)

Moderate to broad (diverse classes of pests for certain products)

Ease of use Low (careful handling and planning of use required)

Moderate to high Highg (same as for conventional pesticides)

High

Compatibility with conventional pesticides

Low (only in certain combinations)

High (not affected by conventional methods)

High High

Cost of application High Highh Low to moderate Variable, but generally low

Effectiveness i Low to moderate Moderate to high Moderate to high High

Adverse effects on human health and environment

Low Very low Low Variable, but sometimes high

a Some insects can be kept for months if conditioned to remain dormant.b Some Bt products are stable for more than three years if frozen or formulated in oil.c Generally a season or less, although release of certain insects into a new area can last for years.d Field persistence of microbial pesticides is usually considered to be short relative to that of conventional pes-ticides. Some, however, such as seed treatments, which will persist until the crop is harvested, provide morelasting control than comparable conventional pesticides.e Certain predator species, however, may be effective against a variety of pests.f Some newer viruses have a broader spectrum.g Some viruses are harder to apply.h Low to moderate, if cost is compared with the cost of custom pesticide application (equipment use and depre-ciation, labor, worker protection training, etc.).i Effectiveness as judged against performance criteria of conventional pesticides.

SOURCE: Office of Technology Assessment, U.S. Congress, 1995.

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rather than the smaller markets usually served byBBTs.

Some analysts predict that the appeal of BBTswill diminish further when the new chemicalscurrently poised for commercialization comeonto the market, for some will compete directlywith Bt (33). The agrochemical industry’s annualR&D investment of more than $2.6 billion is notinsignificant, especially in comparison with theestimated $100 million that goes to private sectorR&D on BBT products (149). Some in the agro-chemical industry believe that they are closingthe gap with newer chemicals that are more envi-ronmentally acceptable and have better toxico-logical profiles. One example is Bayer/Miles’Imidicloprid described by company representa-tives as a “Goldilocks compound. It’s not toohard, not too soft, but just right” (237). Anothernew product, fipronil (a nerve poison), wasdeveloped by analyzing soil for components thattend to deter pests.

Agrochemical companies are pursuing othernew avenues to crop protection as well. Plantsgenetically engineered for pest, pathogen, or her-bicide resistance are perhaps the best example.Many of these will be targeted at major cropsthat provide a potentially large market, such ascotton (96). Metabolites derived from microbes,like Avermectin, are another promising area(33).

Some representatives of the agrochemicalindustry thus believe that the opportunity forBBTs to enter the market in the 1980s and early1990s was somewhat artificial (150). Farmerswere pushed by a lack of alternatives to adopt“next best” methods for pest control, allowing Btand other BBTs to flourish under unique circum-stances. They believe, moreover, that this oppor-tunity will disappear when the BBT productshave to compete with the new chemicals andgenetically engineered plants that are coming online.

❚ ImplicationsThe ambivalent view of BBTs has not been loston long-time participants in the area like the San-

doz Corporation. Such companies are strugglingwith whether to continue investment in this areawhen significant profits are not yet forthcoming.

Overall, agrochemical companies have cometo see BBTs as having their greatest—perhapstheir only—potential in niche markets not wellserved by conventional pesticides (413). Oppor-tunities exist where conventional pesticides arelacking, market size cannot justify the expense ofchemical R&D, highly selective pest control isdesired, or consumers ask for pesticide-free agri-cultural products (413). These are not compara-ble to the “big ticket” markets afforded byconventional pesticides used in corn, wheat, andother major-use crops.

Industry analysts do not expect BBTs to com-pete directly with chemicals, but instead to sup-port their “prudent use” (413). These productsallow companies to maintain a market presencewhere their chemical product sales and distribu-tion networks are already strong (150). Resis-tance management is one of the leading reasonsagrochemical companies have moved to Bt prod-ucts (150). Alternation of BBTs with chemicalmanagement, which slows the rate at whichresistance develops, can prolong the useful lifespan of the chemical. For this reason, some pro-ducers of natural enemies optimistically predict agrowing interest among agrochemical companiesin the marketing of “pest control systems” thatcombine various pest control tools to achieve thedesired level of pest suppression (28). However,few major agrochemical producers have yetdeveloped resistance management as a signifi-cant marketing strategy for BBTs (box 6-2) (79).

Most agrochemical companies have hedgedtheir bets by forming alliances with smaller bio-technology companies rather than developingtheir own R&D programs for BBTs. Throughthese relationships they will realize the benefitsafforded by developing BBT products withoutmaking large-scale investments in the technolo-gies. This approach also puts the agrochemicalcompanies in a good position to take advantageof any major breakthroughs that would bringBBT performance profiles into line with conven-tional products. Such developments could greatly

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expand BBT markets and significantly changethe cost equation for companies deciding whereto invest their resources. Industry representativesbelieve the result would be rapid acquisition ofsmaller biotechnology companies by agrochemi-cal companies (149).

ISSUES AND OPTIONS

❚ Forces Shaping the FutureFuture commercial involvement with biologi-cally based pest control will depend on whetherproducts placed on the market are effective andcost-competitive and whether they match theneeds of growers and other users. Within thesebasic constraints, a wide array of factors willshape the future. Some are more predictable thanothers, and some are influenced by the federalgovernment (table 6-5) (317).

Growth in the public’s demand for organicproduce would probably increase the use ofBBTs, because BBTs are allowed under currentorganic produce certification standards, such asthose promulgated by the California Departmentof Food and Agriculture Organic Program (37A).The Organic Foods Association of North Amer-ica reported that sales of organic products totaled$2.3 billion in 1994, with annual growth exceed-ing 22 percent (226). Conversely, the public’sbasic fear of diseases and microbes could eruptinto concern about use of microbial pesticides.

For example, individual citizens have alreadytried to halt the spraying of Bt by the MarylandDepartment of Agriculture to control Europeangypsy moths (Lymantria dispar) on their prop-erty, despite attempts to educate the public aboutthe virtual nonexistence of any risk to humanhealth (329).

Genetically engineered microbial pesticidesare a wild card in commercial involvement. Themost important issue is whether genetic engi-neering will bring microbial pesticides within theperformance standards of conventional pesti-cides. Public response to the technology also willplay an important role. The release of geneticallyengineered ice-inhibiting microbes in Californiain 1987 caused a furor that has not been forgot-ten. Some industry analysts see the lack of pub-licity in response to the release of geneticallyengineered Bt in California in 1994, similar fieldtests in other states, and now marketing of Raven(a genetically engineered Bt), as a bellwether ofabating public concern (95). Should scientistsdiscover and widely publicize new risks ofgenetically engineered organisms, however, pub-lic opinion could easily turn against use of genet-ically engineered microbes (317).

Changes in the scope and rigor of national andstate environmental policies and pesticide regu-lation could have significant impact. Increasingthe information requirements for pesticide regis-tration could drive up the cost of product regis-

BOX 6-2: How Ciba-Geigy Markets a Microbial Pesticide

Ciba-Geigy has targeted marketing of its Agree Bt-based product to address today’s problems in pestmanagement: pest resistance, environmental impact, and development of IPM systems. According to

Ciba-Geigy’s advertising material on Agree:

Use of Agree will allow the farmer to reduce the amount of neurotoxic insecticides used on a particular

crop. Alternating Agree with neurotoxic insecticides will prolong the effectiveness of both in a resistancemanagement strategy.

As a natural biological, Agree conforms to all IPM objectives: 1) it is host-specific and will not affect

other biotic systems, thus preventing an increase of previously non-threatening pests, while maintainingthe presence of beneficial insects; and 2) it is compatible with most other control methods as a resistance

management tool.

SOURCE: Ciba-Geigy, “All about Agree,” Greensboro, NC, 1995.

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TABLE 6-5: Examples of Factors Potentially Affecting the Future of the BBT Industry

Potential trend, event, or actionPredicted net

effectFederal action that could cause

these effects

Public attitude or perception

Demand for organic foods increases Positive

Public becomes increasingly fearful of diseases and microbes Negative

Public’s suspicions of biotechnology diminish Positive

Media coverage of pesticide hazards increases Positive

Public’s demand for greater food safety grows Positive

Public’s demand for higher standards of environmental safety grows Positive

Industry changes

Natural enemies industry implements voluntary quality control Positive USDA technology transfer or regulatory pressure

Agricultural biotechnology industry collapses under debt load Negative

New, environmentally safe, conventional pesticides are introduced Negative

Crop plants genetically engineered for pest resistance are widely successful

Negative

Farmers increase their reliance on pest control advisors or extension agents knowledgeable about integrated pest management and BBTs

Positive Training of extension agents; licensing/ training of pest control advisors

Growing numbers of food processing companies require low or no pesticide produce from farmers

Positive Changes in food labeling

Farmers’ insurance costs for using pesticides increases Positive

Technology innovations

Cheap, reliable techniques are developed for rearing, packaging, shipping, storing and applying natural enemies

Positive Research or funding via USDA

Production costs for microbial pesticides drop Positive Research or funding via USDA

New pheromone formulations, cheaper methods of synthesis, improved deployment strategies are developed

Positive Research or funding via USDA

Genetic engineering of microbial pesticides results in broader spectrum of activity, enhanced field persistence, or other improvements

Positive Research or funding via USDA

Rate of discovery of novel Bt strains slows down Negative

Natural phenomena

More pests develop resistance to conventional pesticides Positive

Pest resistance to Bt toxins becomes widespread Negative

Public policy

EPA pesticide reregistration process speeds up Positive Internal changes at EPA

Expense of registering or using conventional pesticides grows as a result of provisions in reauthorized Federal Insecticide, Fungicide and Rodenticide Act, Endangered Species Act, or Clean Water Act

Positive Congressional action

More states institute California-type regulation of pesticide use Positive

Coordination between public-sector research and BBT industry increases

Positive USDA or Congress moves to increase coordination

SOURCES: Office of Technology Assessment, U.S. Congress, 1995; A.S. Moffat, “New Chemicals Seek to Outwit Insect Pests,” Science,261(121):550–551, July 30, 1993; K.R. Smith, Henry A. Wallace Institute for Alternative Agriculture, Hyattsville, MD, “Biological Pest Control: AnAssessment of Current Markets and Market Potential,” unpublished contractor report prepared for the Office of Technology Assessment, U.S.Congress, Washington, D.C., January, 1994.

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tration, and thereby further diminish theagrochemical industry’s incentives to invest innew product R&D. Presumably, the result wouldbe a further reduction in the number of conven-tional pesticides on the market and a lack of pes-ticide products for small-market crops like fruitsand vegetables. Such changes would increaseopportunities for biologically based products.Conversely, concern about the potential impactson biodiversity from introducing biological con-trol agents could translate into tightened regula-tion of the natural enemy industry and have adampening effect.

Industry trends also will play a role. Growth ingreenhouse agriculture would probably stimulateincreased use of BBTs, because this is one of themost successful applications of these products.Changes in the capital market that positively ornegatively affect the agricultural biotechnologyindustry could influence the development andavailability of new microbial pesticides, includ-ing genetically engineered ones (317). The extentto which farmers and other users adopt BBTproducts will be a major determinant of marketgrowth. Adoption of BBT products, in turn, maybe affected by technical innovations that increaseproduct efficacy and ease of use, or by the suc-cess of extension agents or pest control advisorsin informing users about BBT products.

❚ Visions of the Future from OTA’s WorkshopOn the theory that best predictions of the futurecome from those with the most experience in thefield, OTA sought the opinions of 12 industryrepresentatives during a workshop held in Sep-tember 1994 (see appendix C). The participantsrepresented the range of companies involved inthe production of biologically based products.OTA asked each workshop member to speculateabout two views of the future—one under thestatus quo and another under the assumption thatthe federal government would take action to sup-port the BBT industry.

Under the Status QuoThe consensus of OTA’s workshop participantswas that, in the absence of any changes to federalprograms or policies, biologically based productswill experience a slow gain in number and uses.Technical improvement in product formulationand efficacy is likely to result gradually inincreased spectrum of efficacy, better handlingand use characteristics, and good incorporationinto IPM programs. Nevertheless, the use ofcommercially available BBTs will increase pri-marily in high value crops such as fruits and veg-etables and other niche areas (e.g., turf,ornamentals, lawn and garden) where current useis greatest. Members of the workshop estimatedthat BBTs might gain as much as 10 to 25 per-cent of those markets where biologically basedproducts are effective (primarily in control ofcertain caterpillar pests).

Economic forces will cause agrochemicalcompanies to continue to work toward “standalone” solutions rather than pest control systems.Consequently, the successful conventional pesti-cides remaining on the market will most likely bebroad-spectrum chemicals that fit poorly intointegrated pest control systems like IPM becausethey may kill natural enemies as well as the tar-get pest. Over time, it will be ever more difficultfor BBTs to compete against the standards set bythese chemicals. This situation, coupled with theincompatibility of the chemicals with integratedpest management, will provide strong incentivesfor farmers to continue with conventional chemi-cally based pest management, especially forthose crops where market size justifies R&Dinvestment (i.e., major use).

An Alternative FutureOTA’s workshop participants also foresaw apossible alternative future in which wider adop-tion of integrated pest management systemswould increase use of BBTs and cause a corre-sponding decrease in the use of conventionalpesticides. Simultaneously, a thriving BBTindustry would be better able to support theseIPM systems by bringing to market a greaterdiversity of BBT products with improved charac-

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❚ Options to Enhance CommercialInvolvement

Commercial development is well advanced for microbial pesti-cides to combat fire blight, a destructive disease of pear andapple trees caused by the bacterium Erwinia amylovora.

Agricultural Research Service, USDA

teristics, such as increased shelf life, ease of use,and efficacy. The driving force behind thesechanges to the status quo would be various fed-eral actions related to regulation, research, tech-nology transfer, and extension.

The workshop’s alternative scenario did notrepresent a radical departure from events underthe status quo. Although participants predicted asmuch as a doubling of market growth rates,under even the most optimistic scenarios BBTswould still amount to only a fraction of the totalmarket by the year 2005 because their presentshare of the pesticide market is so small. Also,the greatest use of BBTs will continue to be out-side the major use crops, which will remain wellserved by the development of new conventionalpesticides.

Nevertheless, the workshop participants sawsuch changes as an integral component of thegovernment’s role in expanded applications ofIPM. In the absence of change, incentives for thepesticide industry will continue to be stacked infavor of the development and marketing ofbroad-spectrum chemicals that are incompatiblewith IPM. And the future of the agriculturalbiotechnology companies, whose R&D hasfueled development of diverse BBT products,will remain uncertain.

The essential choice before Congress, then, iswhether to nurture the BBT industry. Congresscould choose to do this in a number of ways. Thefederal government exerts many subtle and directeffects on the BBT industry (table 6-5 presentedearlier). In this section, OTA identifies a widerange of areas where Congress could adjust thefederal role. These options, by and large, are notlinked; most could be implemented indepen-dently. Because each has an incremental impact,the greatest effect would be felt if a number wereput in place simultaneously.

Regulation has a major impact onBBT companies; it determines which productscan be sold and for what uses, as well as the rela-tive costs of BBT product development and mar-keting. Chapter 4 of this report assesses andpresents options related to the appropriate level,standards, and content of regulatory review. Thatanalysis incorporates considerations related tothe commercial impacts of the regulatory system.Its critical features to the private sector are cost,fairness, and predictability. Industry representa-tives do not view all regulation as undesirable—it can remove poor products from the market-place and address legitimate public concernabout risks (121A,149). However, the currentsystem for BBTs falls down in a number ofplaces. Costs of meeting the information require-ments of regulatory review have a significanteffect on the decisions or ability of companies topursue specific technologies, especially for smallcompanies that produce natural enemies and formidsize biotechnology firms. In addition, futureregulatory requirements are uncertain withrespect to interstate distribution of natural ene-mies and to registration of microbial pesticidesthat have been genetically engineered.

Fashioning Public-PrivatePartnerships in ResearchA lack of dedicated in-house research capabilitiesin the private. sector currently limits R&D of newproducts, production and packaging technologies,

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and delivery systems for certain BBTs. The federalgovernment supports significant related researchthat historically has made important contributionsto the identification of technologies now marketedby the private sector. The level of technology trans-fer has slowed, however, especially in the areas ofnatural enemies and pheromone products.

Some of the ongoing federal research thatmight be of commercial merit seems curiouslyout of sync with the structure of the BBT indus-try. For example, the USDA AgriculturalResearch Service (ARS) and Department ofEnergy scientists recently collaborated on amajor research project to develop ways to mech-anize the rearing of natural enemies (126). Theresult was a series of designs for prototypemachinery that would cost millions of dollarsmore to produce than the total combined annualsales of all natural enemy companies in theUnited States.

Cooperative Research and DevelopmentAgreements (CRADAs) between companies andARS are the major existing mechanism by whichthe private sector buys into ARS efforts (see dis-cussion of ARS in chapter 5). Companies usuallycontribute funds for the research, while ARS pro-vides the scientists and the infrastructure. Underprovisions of the Technology Transfer Act,6

ARS scientists can patent discoveries resultingfrom their work, including research conductedunder a CRADA. Patented discoveries can thenbe licensed for a fee to companies for commer-cialization.

According to representatives of smaller BBTcompanies, the system allows most benefits ofpublic-sector research to accrue to those compa-nies having the greatest financial resources. Para-doxically, these are also the big agrochemicalcompanies having the best access to researchresources of biotechnology companies through avariety of contractual arrangements. Few pastCRADAs have involved the smaller naturalenemy and pheromone companies (300) becausethey lack financial resources to invest in

6 Federal Technology Transfer Act, P.L. 99-502.

research. Although funding by the private sectorpartner is not required for a CRADA, companiesusually provide anywhere from several to over ahundred thousand dollars per agreement (300). Inaddition, representatives of the smaller compa-nies assert that licensing of patented federal dis-coveries has a significant drawback: Somediscoveries have never been developed by thelicensees, although ARS does have the option ofrevoking licenses when this occurs.

ARS announces the availability of opportuni-ties to license new technologies in the FederalRegister and the Commerce Business Daily. Theagency has also just begun to post this informa-tion on the Internet. Nevertheless, small BBTcompanies say they have not had good access tosuch information in the past (17). ARS hasrecently begun to explore additional ways toincrease the frequency with which ARS discov-eries are commercialized by U.S. companies(417A). Posting announcements in informationsources more directly connected to the industrymight improve dissemination to the widest rangeof interested companies.

Congress could instruct ARS to make alldiscoveries related to development and commercial-ization of certain BBTs public property (i.e., not allowARS scientists to patent their discoveries). Areas ofparticular significance to industry are the develop-ment of artificial diets for natural enemies and of newpheromone formulations. The ARS scientists involvedmight need additional incentives to continue researchin these areas. This approach would not be desirablefor microbial pesticides, however, because largercompanies view the licensing arrangement as vitalprotection of intellectual property.

Congress could instruct ARS to encour-age the development of CRADAs even with compa-nies that cannot provide funding for the research. Theagency would need to provide internal incentives andsupport for scientists that engaged in such projects.

Through its oversight functions, Con-gress could encourage ARS to communicate discov-

OPTION

OPTION

OPTION

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Chapter 6 Commercial Considerations 165

cries of relevant technologies and opportunities forcollaborative ventures more effectively to all membersof the BBT industry. Better communication, perhapsvia joint conferences or meetings, might have theadditional benefit of better informing ARS scientists ofthe potential end uses of their discoveries (see chap-ter 5).

Enhancing Opportunities for New ProductsThese are financially troubled times for many ofthe companies that develop and sell BBT prod-ucts. Many relatively small companies operate ata low profit margin and have difficulty investingin product discovery or production technologies.Agricultural biotechnology companies—theoriginators of many innovations in microbialpesticides--depend on a supply of venture capi-tal that is rapidly dwindling. Some of these com-panies are entering a critical period when theirneed for funding will jump, as products longunder development reach the market. The invest-ment algorithm of larger agrochemical compa-nies works against BBT products, with theirniche markets and performance characteristicsthat differ greatly from those of conventionalpesticides. Small-scale infusions of capitalthrough loans, grants, or tax credits might signif-icantly enhance companies’ ability to profitablybring new products to market.

O P T I O N Congress cou ld suppor t research,

development, and launching of new BBT products byproviding tax credits or targeted small-businessloans.

OPTION Congress could enhance market oppor-

tunities for BBT products by punitive regulation ofconventional pesticides or by progressive incentivesdirected toward farmers and other users (see chapter5). Note that the private sector views losses of con-ventional pesticides through regulation and pestresistance as “windows of opportunity” for entry ofbiologically based products into the market. Membersof the industry, however, generally oppose artificialinflation of these opportunities through overly strin-gent regulation of conventional pesticides. They pre-fer policy actions that would affect market sizethrough education and incentives for growers.

Many microbial agents have been registered by EPA, but arenot presently on the market. The celery looper virus is one thatis effective against a number of pests like this cabbage looper(Trichoplusia ni).

Agricultural Research Service, USDA

OPTION Congress could increase the options for

the industry to protect its discoveries as intellectualproperty. Possibilities might include creating new stat-utory mechanisms to patent microbial pesticides (sim-ilar to the P/ant Variety Protection Act), changing thetiming of protection so that it starts at product regis-tration rather than discovery, and financially support-ing patent applications.

OPTION Congress created the Inter-regional

Project No. 4 (IR-4) to support research that developsdata for registration of minor use pesticides. Since thescope of IR-4 was expanded in 1982 to cover “biora-tional” pesticides, only a small part of the program’sfunding has gone towards work on BBTs (see chapter

5). Congress could specify that a larger portion of theIR-4 program funds should be designated to helpmeet the data requirements for registration of micro-bial pesticides and pheromone-based products.

To a significant extent, the instability of theBBT industry stems from uncertain or volatile

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markets. Better education of users about BBTsmight help expand more predictable markets forbiologically based products, as might greaterconsistency of product performance (especiallyfor natural enemies). Options related to user edu-cation are covered in chapter 5.

The quality and purity of natural enemyproducts is thought to vary. Some scientists have sug-gested that APHIS should regulate this area toimprove the consistency of product performance.However, APHIS currently lacks jurisdiction to issuesuch standards. Industry organizations such as theAssociation of Natural Bio-Control Producers and theInternational Organization for Biological Control havebegun to examine issues related to quality control,and the industry is moving toward voluntary stan-dards. Congress could instruct APHIS to work with thenatural enemy industry to develop such standardsand to further assist in these efforts by providingaccess to the scientific resources of USDA.

The federal government itself could provide amajor market for BBTs—especially natural ene-mies—through its pest management programs.Recent experience in Canada has shown that cre-ation of significant potential markets can spurprivate-sector investment. Banning of aerial pes-ticide application in Ontario forests in 1986 mayhave been the impetus for large companies toinvest in the development of Bts for spruce bud-worm control (Nova Nordisk, Zeneca) and massrearing facilities for Trichogramma production(Ciba-Geigy) (318).

Congress could provide market opportu-nities for the natural enemy industry by contractingout the production of biological control agents used infederal pest control programs conducted by APHISand the land management agencies. These agentsare currently produced by federal laboratories.

OPTIONOPTION

OPTIONOPTION

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A

Appendix A:List of Boxes,Figures, and

Tables

❚ Chapter 2: The ContextBox 2-1: Scope of the OTA AssessmentBox 2-2: What Is Integrated Pest Management?Box 2-3: Alar: A Case Study on the Influence of

Public OpinionBox 2-4: Congress Anticipates Future Pest Con-

trol Needs in the 1990 Farm BillBox 2-5: Technologies Not Covered in This

Assessment Also Receiving IncreasedAttention

Table 2-1: Roles of Federal Agencies Related toBiologically Based Pest Control and Loca-tion of Discussion in This Report

Table 2-2: User Expenditures for Pesticides inthe U.S. by Sector, 1993

Table 2-3: Use of Integrated Pest Managementon U.S. Crops

Table 2-4: Critical Cases of Multiple InsecticideResistance in the U.S. Today

Figure 2-1: Growth in U.S. Conventional Pesti-cide Use, 1964 to 1993

Figure 2-2: Approaches to Pest Control in Prac-tice Today

❚ Chapter 3: The TechnologiesBox 3-1: Outcomes of Biologically Based Pest

Control

Box 3-2: How Changes in Available PesticidesAffect Adoption of BBTs

Box 3-3: How Conservationists are Turning toBiological Control to Help Save Biodiver-sity

Box 3-4: The Areawide Pest Management Con-cept

Box 3-5: The Message from Experts Remains theSame, but Progress in Bringing BBTs intoUse Has Been Slow

Table 3-1: Available Data on the Use of BBTs inthe U.S.

Table 3-2: Priority Research Needs Identified byOTA’s Contractors

Figure 3-1: Intervention is Not Always Necces-sary to Prevent Unwanted Pest Damage

Figure 3-2: Adoption of Biointensive IPM byMajor Food Companies

Figure 3-3: Key Stages of BBT Research, Devel-opment, and Implementation

❚ Chapter 4: Risks and RegulationsBox 4-1: Controlling Public Health Scourges

with BBTsBox 4-2: Regulation of BBTs by Hawaii and

Other StatesBox 4-3: Oversight of Vertebrates as Biological

Control Agents

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Box 4-4: The Proposed APHIS Regulation forthe Introduction of Nonindigenous Organ-isms

Box 4-5: Pest Control ActsBox 4-6: Categories of Pest OrganismsBox 4-7: Technical Advisory Group on the Intro-

duction of Biological Control Agents ofWeeds

Box 4.8 Chronology of the Praxis Company’sExperience with FDA

Box 4-9: Other Regulatory SystemsTable 4-1: Examples of Potential Risks from

BBTsTable 4-2: Categories Regulated by EPA

❚ Chapter 5: From Research to ImplementationBox 5-1: USDA’s Integrated Pest Management

InitiativeBox 5-2: Case Studies of USDA Pest Control

Programs Involving Biologically BasedTechnologies

Box 5-3: California Taking an Active Role inChanging Pest Management Practices

Box 5-4: Campbell Soup CompanyBox 5-5: Connection between Research and

Implementation in AustraliaTable 5-1: Funding for Research on BBTsTable 5-2: Funding of BBT-Based Pest Control

ProgramsTable 5-3: Technologies Used in Pest Manage-

ment Programs of the Animal and PlantHealth Inspection Service (USDA)

Figure 5-1: General Schematic of the DecisionProcesses by which the AgriculturalResearch Service and State AgriculturalExperiment Stations Award Research Funds

Figure 5-2: Biological Control Expenditures andPrograms in State Departments of Agricul-ture

Figure 5-3: Distribution of Federal BBTResearch According to Pest Type (1994)

❚ Chapter 6: Commercial ConsiderationsBox 6-1: Biologically Based Products for Pest

ControlBox 6-2: How Ciba-Geigy Markets a Microbial

PesticideTable 6-1: Estimated Market Value of Biologi-

cally Based Pest Control Products (millionsof dollars annually: 1990, 1991, or 1992)

Table 6-2: Projection: How Improved Productionand Handling Technologies Would Incre-mentally Increase the Scale and Decrease theCosts of Trichogramma Production

Table 6-3: Examples of Biologically Based Prod-ucts Marketed by Major Agrichemical Com-panies or Their Partners

Table 6-4: Comparison of Biologically BasedProducts and Conventional Pesticides

Table 6-5: Examples of Factors PotentiallyAffecting the Future of the BBT Industry

Figure 6-1: Comparison of BBT and Conven-tional Pesticide Sales According to Type ofPest

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B

Appendix B:List of

Acronyms

ANBP: Association of Natural Bio-Control Pro-ducers

APHIS: Animal and Plant Health Inspection Ser-vice

ARS: Agricultural Research ServiceASA: American Semiochemicals AssociationBATS: Biological Assessment and Taxonomic

Support (APHIS)BBTs: Biologically Based Technologies (for pest

control)BIO: Biotechnology Industry OrganizationBPPD: Biopesticides and Pollution Prevention

Division (EPA)Bt: Bacillus thuringiensisCRADA: Cooperative Research and Develop-

ment AgreementCSREES: Cooperative State Research, Educa-

tion, and Extension ServiceDALs: Defect Action LevelsDoI: U.S. Department of the InteriorEPA: U.S. Environmental Protection AgencyESA: Entomological Society of AmericaFACA: Federal Advisory Committee ActFDA: U.S. Food and Drug AdministrationFFDCA: Federal Food, Drug and Cosmetic Act

FHP: Forest Health Protection (U.S. Forest Ser-vice)

FIDR: Forest Insect and Disease Research (U.S.Forest Service)

FIFRA: Federal Insecticide, Fungicide, andRodenticide Act

FWS: U.S. Fish and Wildlife ServiceGRAS: Generally Recognized As SafeIBC3: Interagency Biological Control Coordinat-

ing CommitteeIOBC: International Organization of Biological

ControlIPM: Integrated Pest ManagementIR-4: Interregional Research Project No. 4NBCI: National Biological Control Institute

(APHIS)NPV: Nuclear Polyhedrosis VirusNRI: National Research InitiativeOPP: Office of Pesticide Programs (EPA)OTA: Office of Technology AssessmentPPQ: Plant Protection and Quarantine (APHIS)TAG: Technical Advisory Group on the Intro-

duction of Biological Control Agents ofWeeds

USDA: U.S. Department of Agriculture

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C

Appendix C:Background Reports,

Workshops, andWorkshop Participants

BACKGROUND REPORTS:W. Cranshaw, Colorado State University Fort

Collins, CO. Biologically Based Technolo-gies For Pest Control: Urban and SuburbanEnvironments

J.M. Cullen and T.E. Bellas, CSIRO, Canberra,Australia. Australian Laws, Policies andPrograms Related to Biologically BasedTechnologies For Pest Control

M.L. Flint, University of California, Davis, CA.Biological Pest Control: Technology andResearch Needs

G. Georghiou, University of California River-side, CA. Insecticide Resistance in theUnited States

D.M. Gibbons, The EOP Foundation, Inc.,Washington, DC. Report on the Role of theUSDA in Biologically Based Pest ControlResearch

G.E. Harman and C.K. Hayes, Cornell Univer-sity, Ithaca, NY. Biologically Based Tech-nologies For Pest Control: Pathogens ThatAre Pests of Agriculture

J.M. Houghton, Houghton and Associates, St.Louis, MO. Biologically Based TechnolgiesFor Pest Control: Workshop on the Role ofthe Private Sector

J. M. Houghton, Houghton and Associates, St.Louis, MO. The View of Biological PestControl From the Pesticide Industry

A. Kuris, University of California, Santa Bar-bara, CA. A Review of Biologically BasedTechnologies For Pest Control in AquaticHabitats

P.B. McEvoy, Oregon State University, Corval-lis, OR. Testing Biocontrol Agents andMicrobial Pesticides For Host Specificity

W.W. Metterhouse, Cream Ridge, NJ. TheStates’ Roles in Biologically Based Technol-ogies For Pest Control

J.R. Nechols and J.J. Obrycki, Kansas State Uni-versity and Iowa State University, Manhat-tan, KS, and Ames, IA. OTA PreliminaryAssessment of Biological Control: CurrentResearch

P.J. Nowak, University of Wisconsin, Madison,WI. Educating Users About BiologicallyBase Methods of Pest Control

J. Randall and M. Pitcairn, The Nature Conser-vancy, Galt, CA, and the Biological ControlProgram, California Department of Foodand Agriculture, Sacramento, CA. Biologi-cally Based Technologies For Pest Controlin Natural Areas and Other Wildlands

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K. Reichelderfer Smith, Henry A. Wallace Insti-tute for Alternative Agriculture, Hyattsville,MD. Biological Pest Control: An Assess-ment of Current Markets and Market Poten-tial

D. Simberloff and P. Stiling, Florida State Uni-versity, Tallahassee, FL, and University ofSouthern Florida, Tampa, FL. BiologicalPest Control: Potential Hazards

R.G. Van Driesche, T.G. Bellows, O. Minken-burg, M. Adang, B. Federici, C. McCoy, J.Maddox, H. Kaya, J. Lewis, R. Cardé, andE.S. Krafsur, University of Massachusetts,Amherst, MA (Van Driesche, only). Reporton Biological Control of Invertebrate Pestsof Forestry and Agriculture

A.K. Watson, McGill University, Quebec, Can-ada. Biologically Based Technologies ForPest Control: Agricultural Weeds

D. Zilberman and C. Yarkin, University of Cali-fornia, Berkeley, CA. The Economics ofDevelopment and Adoption of Pest ControlProducts With Emphasis on BiologicallyBased Controls

WORKSHOPS:

❚ Preliminary Planning Workshop, December 20–21, 1993

Participants:

Mary Louise FlintCalifornia Statewide IPM ProgramDavis, CA

John HoughtonHoughton AssociatesSt. Louis, MO

James NecholsKansas State UniversityManhattan, KS

Katherine Reichelderfer SmithHenry A. Wallace Institute for Alternative

AgricultureGreenbelt, MD

Daniel SimberloffFlorida State UniversityTallahassee, FL

❚ Role of the Private Sector in Biologically Based Technologies for Pest Control, September 20–21, 1994

Participants:

Jake BlehmBuena Biosystems, Inc.Ventura, CA

Robert CibulskyAbbott LaboratoriesNorth Chicago, IL

Stephen DumfordCiba-Geigy CorporationGreensboro, NC

Janice GillespieTechnology Concep, Inc.Bend, OR

Louie T. HargettSandoz Agro, Inc.Des Plains, IL

William HeilmanAmerican Cyanamid Co.Princeton, NJ

Paul KoppertKoppert B.V.The Netherlands

Pamela G. MarroneNovo Nordisk Entotech, Inc.Davis, CA

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Appendix C: Background Reports, Workshops, and Workshop Participants | 173

John McIntyreEcogen, Inc.Doylestown, PA

Sinthya PennBeneficial InsectaryOak Run, CA

Edwin QuattlebaumBiosysPalo Alto, CA

Todd TaylorCrop Genetics InternationalColumbia, MD

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DAppendix D:

Reviewers

REVIEWERS OF THE FULL ASSESSMENT

Janet AndersonU.S. Environmental Protection AgencyAlexandria, VA

David AndowUniversity of MinnesotaSt. Paul, MN

Paul A. BackmanAuburn UniversityAuburn, AL

Ring T. CardéUniversity of MassachusettsAmherst, MA

Robert J. CibulskyAbbott LaboratoriesNorth Chicago, IL

Ernest S. DelfosseAnimal and Plant Health Inspection ServiceU.S. Department of AgricultureHyattsville, MD

Willard A. DickersonNorth Carolina Department of AgricultureRaleigh, NC

Patricia J. DuranaOffice of Technology AssessmentEnvironment Program

Roger C. FunkThe Davey Tree Expert CompanyKent, OH

Harry J. GriffithsEntomological Services Inc.Corona, CA

Judith A. HansenCape May County Mosquito Extermination

CommissionCape May, NJ

Dennis L. IsaacsonOregon Department of AgricultureSalem, OR

Tobi L.JonesCalifornia Environmental Protection AgencySacramento, CA

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Peter M. KareivaUniversity of WashingtonSeattle, WA

Allen E. KnutsonTexas Agricultural Extension ServiceCollege Station, TX

David W. MillerEcoScience Corp.Northborough, MA

Timothy L. NanceGro Technics ConsultingNaples, FL

Katherine Reichelderfer SmithHenry A. Wallace Institute for Alternative

AgricultureGreenbelt, MD

David O. TeBeestUniversity of ArkansasFayetteville, AR

Jeffrey K. WaageInternational Institute of Biological ControlAscot, Berks, UK

Michael E. WetzsteinUniversity of GeorgiaAthens, GA

David M. WhitacreSandoz Agro, Inc.Des Plaines, IL

REVIEWERS OF A PORTION OF THE ASSESSMENT OR BACKGROUND REPORT

Janet AndersonU.S. Environmental Protection AgencyAlexandria, VA

David AndowUniversity of MinnesotaSt. Paul, MN

Gregory H. ApletThe Wilderness SocietyWashington, DC

William BeckNovo Nordisk Bioindustrials, Inc.Danbury, CT

Fred BetzJellinek, Schwartz & Connolly, Inc.Washington, DC

Tom BewickUniversity of FloridaGainesville, FL

Larry G. BezarkCalifornia Department of Food and AgricultureSacramento, CA

Jake BlehmBuena BiosystemsVentura, CA

Neal J. BriggiNovo Nordisk Bioindustrials, Inc.Danbury, CT

Ring T. CardéUniversity of MassachusettsAmherst, MA

Gerald A. CarlsonNorth Carolina State UniversityRaleigh, NC

James R. CateCooperative State Research ServiceU.S. Department of AgricultureWashington, DC

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Appendix D: Reviewers | 177

Robert J. CibulskyAbbott LaboratoriesNorth Chicago, IL

Whitney CranshawColorado State UniversityFort Collins, CO

James CullenCSIROCanberra, Australia

Donald L. DahlstenUniversity of CaliforniaBerkeley, CA

Ernest S. DelfosseAnimal and Plant Health Inspection ServiceU.S. Department of AgricultureHyattsville, MD

Willard A. DickersonNorth Carolina Department of AgricultureRaleigh, NC

L.E. EhlerUniversity of CaliforniaDavis, CA

Raymond EidWilmington, DE

David A. FischhoffMonsanto CompanySt. Louis, MO

Mike FitznerCooperative State Research, Extension, and

Education ServiceU.S. Department of AgricultureWashington, DC

Mary Louise FlintUniversity of CaliforniaDavis, CA

Lyle B. ForerPennsylvania Department of AgricultureHarrisburg, PA

J. Howard FrankUniversity of FloridaGainesville, FL

James R. FuxaLouisiana State UniversityBaton Rouge, LA

Ramon GeorgisBiosysPalo Alto, CA

Harry J. GriffithsEntomological Services Inc.Corona, CA

Philip J. HammanTexas A&M UniversityAustin, TX

Judith A. HansenCape May County Mosquito Extermination

CommissionCape May, NJ

Louie T. HargettSandoz Agro, Inc.Des Plaines, IL

Gary HarmanCornell UniversityIthaca, NY

Peter HarrisAgriculture and Agri-Food CanadaLethbridge, Alberta, Canada

William P. HeilmanAmerican Cyanimid CompanyPrinceton, NJ

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Michael HoffmanCornell UniversityIthaca, NY

John M. HoughtonJ.M. Houghton and AssociatesSt. Louis, MO

Francis G. HowarthBishop MuseumHonolulu, HI

Charles R. HowellAgricultural Research ServiceCollege Station, TX

Marjorie A. HoyUnversity of FloridaGainesville, FL

John W. ImpsonCooperative State Research, Education, and

Extension ServiceU.S. Department of AgricultureWashington, DC

Dennis L. IsaacsonOregon Department of AgricultureSalem, OR

Barry JacobsonU.S. Department of AgricultureWashington, DC

Wojciech JanisiewiczAgricultural Research ServiceU.S. Department of AgricultureKernsville, WV

Tobi JonesCalifornia Environmental Protection AgencySacramento, CA

Erik D. KiviatHusoniaAnnandale, NY

W. KlassenUniversity of FloridaHomestead, FL

Allen E. KnutsonTexas Agricultural Extension ServiceCollege Station, TX

Karen KoltesNational Biological ServiceWashington, DC

James L. KrysanAgricultural Research ServiceU.S. Department of AgricultureBeltsville, MD

P.J. KuchAgriculture Policy BranchU.S. Environmental Protection AgencyWashington, DC

Armand KurisUniversity of CaliforniaSanta Barbara, CA

Norman LepplaAnimal and Plant Health Inspection ServiceU.S. Department of AgricultureBeltsville, MD

Anne R. LeslieOffice of Prevention, Pesticides and Toxic

SubstancesU.S. Environmental Protection AgencyWashington, DC

Hiram LiOregon State UniversityCorvallis, OR

Jeffrey A. LockwoodUniversity of WyomingLaramie, WY

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Appendix D: Reviewers | 179

Michelle C. MarraNorth Carolina State UniversityRaleigh, NC

Pamela G. MarroneNovo Nordisk Entotech, Inc.Davis, CA

Arthur H. MasonMinnesota Department of AgricultureSt. Paul, MN

Peter McEvoyOregon State UniversityCorvallis, OR

John McIntyreDoylestown, PA

Robert L. MetcalfUniversity of CaliforniaRiverside, CA

William MetterhouseCream Ridge, NJ

Dale MeyerdirkAnimal and Plant Health Inspection ServiceU.S. Department of AgricultureBeltsville, MD

David W. MillerEcoScience Corp.Northborough, MA

James R. NecholsKansas State UniversityManhattan, KS

John J. ObryckiIowa State UniversityAmes, IA

Eldon E. OrtmanPurdue UniversityWest Lafayette, IN

Sinthya PennBeneficial InsectaryOak Run, CA

Carol G. PetersonOffice of Pesticide ProgramsU.S. Environmental Protection AgencyWashington, DC

P.C. Quimby, Jr.Agricultural Research ServiceU.S. Department of AgricultureBozeman, MT

John RandallThe Nature ConservancyDavis, CA

Tom RobertsBureau of Land ManagementU.S. Department of the InteriorWashington, DC

Sally J. RockeyCooperative State Research, Education, and

Extension ServiceU.S. Department of AgricultureWashington, DC

Matthew RoyerAnimal and Plant Health Inspection ServiceU.S. Department of AgricultureBeltsville, MD

J. Thomas SchmidtNovo Nordisk Bioindustrials, Inc.Danbury, CT

Esther SchneiderNational Biological ServiceU.S. Department of the InteriorWashington, DC

Milton N. SchrothUniversity of CaliforniaBerkeley, CA

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Jeffrey G. ScottCornell UniversityIthaca, NY

Daniel SimberloffFlorida State UniversityTallahassee, FL

R.D. SjobladOffice of Pesticide ProgramsU.S. Environmental Protection AgencyWashington, DC

Robert D. SjogrenMeridian Precision Release TechnologiesMinneapolis, MN

Katherine Reichelderfer SmithHenry A. Wallace Institute for Alternative

AgricultureGreenbelt, MD

Judith B. St. JohnAgricultural Research ServiceU.S. Department of AgricultureBeltsville, MD

David O. TeBeestUniversity of ArkansasFayetteville, AR

Jay TroxelFish and Wildlife Management AssistanceU.S. Fish and Wildlife ServiceArlington, VA

Charles E. TurnerAgricultural Research ServiceU.S. Department of AgricultureAlbany, CA

Roy G. Van DriescheUniversity of MassachusettsAmherst, MA

Mike WallaceTexas Pest Management AssociationAustin, TX

William S. WallaceAnimal and Plant Health Inspection ServiceU.S. Department of AgricultureWashington, DC

Lewis WatersBureau of Land ManagementU.S. Department of the InteriorWashington, DC

Pat W. WeddleWeddle, Hansen and Associates, Inc.Placerville, CA

David M. WhitacreSandoz Agro, Inc.Des Plaines, IL

H. Alan WoodBoyce Thompson Institute for Plant Research,

Inc.Ithaca, NY

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References

1. “Adulterated Food” (342(a)(3)), Title 21(Food and Drugs 1 to 800) U.S. Code, 1972ed.

2. “Agricultural Experiment Stations” (361(a)to 361(i)), Title 7 (Agriculture 281 to 1099)U.S. Code, 1980 ed.

3. “Agricultural Research Program” (450(i)),Title 7 (Agriculture: 281 to 1099) U.S. Code,1980 ed.

4. Aldhous, P., “Malaria: Focus on MosquitoGenes,” Science 261(121):646–648, July 30,1993.

5. Alms, M.J., National Alliance of Indepen-dent Crop Consultants and Blue Earth Agro-nomics, Inc., Lake Crystal, MN, personalcommunication, August 15, 1995.

6. Alms, M.J., “Challenges for IPM in theFuture: An Independent Crop Consultant’sPerspective,” Second National IntegratedPest Management Symposium/Workshop—Proceedings (Raleigh, NC: UniversityGraphics, 1994).

7. American Society of Agronomy, NationalCertified Crop Advisor—PerformanceObjectives, 1995.

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