100 YEARS OF Bacillus thuringiensis - IPM Florida

100 YEARS OF

Bacillus thuringiensis:A Critical Scientific Assessment

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Copyright © 2002American Academy of Microbiology1752 N Street, NWWashington, DC 20036

This report is based on a colloquium, “100 Years of Bacillis thuringiensis, a Paradigm forProducing Transgenic Organisms: A Critical Scientific Assessment,” sponsored by theAmerican Academy of Microbiology and held November 16-18, in Ithaca, New York.

The American Academy of Microbiology is grateful for the generous support of the fol-lowing organizations:

American Society for MicrobiologyCornell UniversityU.S. Environmental Protection AgencyU.S. Food and Drug AdministrationNational Science FoundationRockefeller Foundation

The opinions expressed in this report are those solely of the colloquium participants.

This report and others from the American Academy of Microbiology are available online: www.asmusa.org

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100 Years of Bacillus thuringiensis ■ 1

A report from the American Academy of Microbiology

100 YEARS OF

Bacillus thuringiensis:A Critical Scientific Assessment

EUGENE W. NESTERLINDA S. THOMASHOW

MATTHEW METZ AND

MILTON GORDON

A report from the American Academy of Microbiology

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2 ■ 100 Years of Bacillus thuringiensis

Board of Governors, American Academy of MicrobiologyEugene W. Nester, Ph.D. (Chair), University of Washington

Joseph M. Campos, Ph.D., Children’s National Medical Center

R. John Collier, Ph.D., Harvard Medical School

Marie B. Coyle, Ph.D., University of Washington

James E. Dahlberg, Ph.D., University of Wisconsin, Madison

Julian E. Davies, Ph.D., Cubist Pharmaceuticals, Inc.

Arnold L. Demain, Ph.D., Drew University

Lucia B. Rothman-Denes, Ph.D., University of Chicago

Abraham L. Sonenshein, Ph.D., Tufts University Medical Center

David A. Stahl, Ph.D., University of Washington

Judy D. Wall, Ph.D., University of Missouri

Colloquium Steering CommitteeEugene W. Nester, Ph.D. (Co-Chair), University of Washington

Linda S. Thomashow, Ph.D. (Co-Chair), USDA/

Washington State University

Luca Comai, Ph.D., University of Washington

Milton Gordon, Ph.D., University of Washington

Noel Keen, Ph.D., University of California, Riverside

Anne M. Vidaver, Ph.D., University of Nebraska

Carol A. Colgan, American Academy of Microbiology

Colloquium ParticipantsMichael Adang, Ph.D., University of Georgia

Illimar Altosaar, Ph.D., University of Ottawa

Arthur I. Aronson, Ph.D., Purdue University

Lee A. Bulla, Ph.D., University of Texas, Dallas

Christopher Cullis, Ph.D., National Science Foundation

Peter R. Day, Ph.D., Rutgers University

Donald H. Dean, Ph.D., Ohio State University

Elizabeth D. Earle, Ph.D., Cornell University

David J. Ellar, Ph.D., University of Cambridge, England

Brian A. Federici, Ph.D., University of California, Riverside

Sarjeet S. Gill, Ph.D., University of California, Riverside

Milton Gordon, Ph.D., University of Washington

Peter M. Kareiva, Ph.D., The Nature Conservancy

John D. Kemp, Ph.D., New Mexico State University

Pal Maliga, Ph.D., Rutgers University

Michelle Marvier, Ph.D., Santa Clara University

Sharlene Matten, Ph.D., U.S. Environmental Protection Agency

Matthew Metz, Ph.D., University of Washington

William Moar, Ph.D., Auburn University

Eugene W. Nester, Ph.D., University of Washington

Sheikh Riazzuddin, Ph.D., National Centre of Excellence in

Molecular Biology, Lahore, Pakistan

Ronald R. Sederoff, Ph.D., North Carolina State University

Anthony M. Shelton, Ph.D., Cornell University

Allison Snow, Ph.D., Ohio State University

Diane Stanley-Horn, Ph.D., University of Guelph

Guenther Stotzky, Ph.D., New York University

Linda S. Thomashow, Ph.D., USDA/Washington State University


are equally amenable to use in large orsmall scale farming operations and com-patible with other agricultural practicesand technologies.

Concerns associated with the use of Btinclude potential for harm to non-targetorganisms, development of resistance inpopulations of target insects, and, forengineered crops, possible ecologicalconsequences of gene flow to non-engi-neered crops and wild relatives. Theseconcerns merit continued attention on acase-by-case basis in order to ensurethat Bt technologies have the maximumpositive impact with a minimum risk onagriculture. Prudent use of Bt technolo-gies will also be key in maintaining theirusefulness for a long period of time.

Executive SummaryThe insecticidal proteins produced byBacillus thuringiensis (Bt) have provideda uniquely specific, safe, and effectivetool for the control of a wide variety ofinsect pests. Bt has been used in sprayformulations for over 40 years, where itis considered remarkably safe, in largepart because specific formulations harmonly a narrow range of insect species.Today, Bt insecticidal protein geneshave been incorporated into severalmajor crops where they provide a modelfor genetic engineering in agriculture.

Effective protection of crops from insectpests afforded by insecticidal proteinshas had a number of positive impactson agriculture. Reduced insect damageim-proves crop yield, reduces fungaltoxins in the food supply, and improvesthe livelihood of farmers. Replacementof toxic chemical pesticides with Bt hasreduced hazards to the environmentand farm workers. Bt-engineered crops




BackgroundIntroduction of transgenic crops hasprovided new approaches to improvingcrop quality and productivity, but, atthe same time, these crops havearoused concerns about the safety ofagricultural biotechnology in relation tohuman health and the environment.These issues are, for the most part, relevant to agricultural practices ingeneral, and are embodied in cropsengineered to produce an insecticidalprotein from the common bacteriumBacillus thuringiensis (Bt).

The insecticidal properties of B. thurin-giensis have long been recognized.While some accounts indicate that theEgyptians were aware of the insecticidalproperties of what probably was Bt andused it to control pests, the organismwas first isolated about 100 years ago inJapan from silkworm larvae sufferingfrom the disease “flacherie.” The organ-ism was named Bacillus thuringiensis byBerliner in 1911, who isolated it from adiseased flour moth larva. In 1954, Angusdemonstrated that the crystalline proteininclusions produced by B. thuringiensisin the course of sporulation were re-sponsible for the insecticidal action.

Insecticidal products of Bt were firstcommercialized in France in the late1930s. For over 40 years Bt has beenapplied to crops as an insecticidal spray,a mixture of spores and the associatedprotein crystals. By 1995, 182 Bt prod-ucts were registered by the UnitedStates Environmental Protection Agency(EPA), but in 1999 Bt formulations con-stituted less than two percent (2%) ofthe total sales of all insecticides. Theuse of Bt has increased as insects havebecome resistant to chemical insecti-cides. Recently, the use of Bt in pestcontrol has increased substantiallythrough more widespread use by bothconventional and “organic” food produc-ers, as well as in forestry.

In 1987, three reports were publishedthat demonstrated that insecticidalcrystal protein (ICP) genes from Btcould be introduced and expressed inthe tissues of tobacco and tomato,resulting in pest-resistant transgenicplants. By 2001, an estimated 69% ofthe cotton, 26% of the corn, and 68% ofthe soybeans grown in the UnitedStates were genetically engineered. Forcotton and corn, the genetic engineer-ing has involved the introduction of Btgenes into these crops to confer insectresistance. Thus, Bt serves as a para-

digm for transgenic plants. A timeline(Figure 1) highl ight ing importantevents in the development of Bt as aninsecticide is given.

The unprecedented and rapid adoption of transgenic crops since 1996 hasraised questions among the public, governmental regulatory agencies, envi-ronmental groups, and the scientificcommunity about the potential effectsof these crops on non-target organisms,human health, and non-engineeredcrops or relatives of crop species. Thepotential toxicity of pollen from Bt cornon non-target organisms such as themonarch butterfly, the prospect of trans-genic plants attaining special allergenicor toxic properties, and possible conse-quences of gene flow on crop geneticdiversity and weed hardiness are someof the safety issues that have receivedattention in recent years. Other con-cerns are societal, and encompassimpacts of the technology on interna-tional trade policy and cultural values.

Twenty-five (25) scientists with exper-tise in various aspects of Bt, plantbiology, entomology, microbiology, andecology were convened for a 2-1/2 daycolloquium to address objectively thescientific basis surrounding these andother concerns about the safety and

FIGURE 1. TIMELINE OF IMPORTANT EVENTS IN THE DEVELOPMENT OF Bt AS AN INSECTICIDE.

1901

•ISHIWATA

SHIGETANE

DISCOVERS

THAT A

DISEASE OF

SILKWORMS IS

CAUSED BY A

PREVIOUSLY

UNDESCRIBED

BACTERIUM

1911

•E. BERLINER

NAMES THE

ORGANISM

CAUSING THE

DISEASE IN

SILKWORM—

BACILLUS

THURINGIENSIS

(Bt)

1938

•THE FIRST

COMMERCIAL

PRODUCTS

THAT CONTAIN

Bt ARE

MARKETED IN

FRANCE

1954

•T. ANGUS

SHOWS THAT

CRYPTALLINE

PROTEINS ARE

RESPONSIBLE

FOR

INSECTICIDAL

ACTION OF Bt

1983

•SCIENTISTS

DEMONSTRATE

THAT PLANTS

CAN BE

GENETICALLY

ENGINEERED

1987

•PEST

RESISTANCE

OF PLANTS

CONTAINING

THE Bt GENE

DEMON-

STRATED

1996

•Bt COTTON

REACHES THE

MARKET

2001

•IN THE U.S.

69% OF THE

COTTON, AND

26% OF THE

CORN PLANTED

CONTAIN

Bt GENES


each other than to isolates in other clus-ters, these analyses indicate that B.anthracis is genetically distinct from B.thuringiensis and B. cereus. This emer-ging picture of genetic relationships isconsistent with what is known of theecology of these species: B. thuringien-sis and B. cereus are indigenous tohabitats in and around soil and insects,whereas B. anthracis is restricted togrowth in animal hosts because of itsobligately pathogenic lifestyle.

presence in B. thuringiensis of parasporalcrystals, but this is now considered toonarrow a criterion for taxonomic pur-poses. A clearer understanding of therelationships among these organismshas begun to emerge, based on theapplication of high-resolution analyses of the genetic variability among largenumbers of isolates. Isolates of B. thurin-giensis and B. cereus are highly diverse,whereas very little genetic variationexists among isolates of B. anthracis.Thus, when isolates are grouped in aphylogenetic tree on the basis of geneticsimilarity, isolates of B. anthracis aretightly clustered. In contrast, isolates ofB. thuringiensis and B. cereus form sev-eral different clusters that containisolates from both species. Because iso-lates within a cluster are more similar to

environmental consequences of Btcrops, particularly as compared withalternatives, such as conventional Btsprays and synthetic insecticides. Thisreport summarizes the conclusionsreached in their discussions.

Bt’s Family TreeBt is a member of the genus Bacillus, a diverse group of gram-positive, aerobic, spore-forming bacteria consist-ing of more than 20 species that differ intheir basic biological properties. In addi-tion to Bt, the most important speciesare B. subtilis, a source of industrialenzymes; B. cereus; and B. anthracis, thecausative agent of anthrax. Members ofthe genus Bacillus generally are consid-ered soil bacteria, and Bt is common interrestrial habitats, including soil, livingand dead insects, insect feces, granaries,and on the surfaces of plants. Bt occursin nature predominantly as spores thatcan disseminate widely throughout theenvironment. B. anthracis also survivesas spores, but there is no evidence oftoxin gene transfer from B. anthracis toB. thuringiensis or B. cereus.

B. thuringiensis, B. cereus, and B. anthra-cis are closely related. Until recentlythey were differentiated based on bio-chemical, nutritional, and serologicalanalyses, on the presence in Bt of insec-ticidal parasporal crystals visible bymicroscopy (Figure 2), and on patho-genicity to mammals. Insecticidalactivity and pathogenicity in animalsdepend, in part, on the presence in B. thuringiensis and B. anthracis of plas-mids, but the plasmids in the twospecies differ functionally and geneti-cally, and those present in B. anthracishave never been found to be transferredto other species of Bacillus.

Accumulated molecular evidence sug-gests that B. thuringiensis and B. cereusshould be considered a single species.They have been distinguished by the


FIGURE 2. THE INSECTICIDAL BACTERIUM, BACILLUS THURINGIENSIS. A. CELL OF

B. THURINGIENSIS IN THE PROCESS OF SPORULATION, DURING WHICH INSECTI-

CIDAL PROTEINS ARE PRODUCED AND CRYSTALLIZE. B. PARASPORAL CRYSTALS

ISOLATED FROM THE HD1 ISOLATE OF B. THURINGIENSIS SUBSP. KURSTAKI (BTK).

THE HD1 ISOLATE OF PRODUCES FOUR MAJOR CRY PROTEINS, CRY1Aa,

CRY1Ab, CRY1Ac, AND CRY2Aa, AND IS USED WIDELY IN AGRICULTURE AND

FORESTRY TO CONTROL CATERPILLAR PESTS. C. A PARASPORAL CRYSTAL OF B.

THURINGIENSIS SUBSP. ISRAELENSIS (BTI). BTI PRODUCES FOUR MAJOR INSEC-

TICIDAL PROTEINS, CRY4Aa, CRY4Ab, CRY11Aa, AND CYT1Aa, AND IS USED TO

CONTROL THE LARVAE OF MOSQUITOES AND BLACKFLIES. E = EXOSPORIUM

MEMBRANE, SP = SPORE, AND PB = PARASPORAL BODY. BAR IN A EQUALS 250

NM, OR ONE 40,000TH OF A CM.



How Does Bt Work?

Various strains and insecticidal proteinsThe diversity within B. thuringiensis isreflected in the fact that more than 60serotypes and hundreds of different sub-species have been described. The twomost widely used in commercial insecti-cides are B. thuringiensis subsp. kurstaki(Btk), which kills a wide range of lepi-dopteran species that are importantpests in agriculture and forestry, and B.thuringiensis subsp. israelensis (Bti),used primarily for the control of mos-quito and blackfly larvae.

Most of the insecticidal activity of Bt isdue to intracellular crystal inclusionsproduced during the process of sporula-tion. These parasporal crystals (Figure 2)are comprised of one or more relatedICPs encoded by cry (crystal) and cyt(cytolytic) genes located mainly on plas-mids. Like B. thuringiensis itself, the cryand cyt genes are highly diverse; morethan 30 types of Cry proteins and 8types of Cyt proteins have beendescribed, and over 100 genes havebeen cloned and sequenced. Targetinsect specificity is determined mainlyby the ICPs, although B. thuringiensisalso produces a variety of otherenzymes and insecticidal proteins that

may contribute to its virulence. Onehundred and twenty six (126) Bt micro-bial insecticides are currently registeredin the US, but these are based on onlyfour subspecies of B. thuringiensis. Onlyfive ICP genes have been engineeredinto commercial Bt crops, but many others are available for future use.

Susceptible organismsInsecticides are generally sought thattarget high-impact agricultural pests,disease vectors, or nuisance pests.Whether applied as a commercial sprayor deployed in crops, Bt is highly spe-cific, with toxicity limited to only somespecies of one of the major groups ofinsects—typically lepidoptera (butter-flies/moths), coleoptera (beetles), ordiptera (flies/mosquitos). New Bt pro-teins are being discovered which areactive against other orders of insectsand other pests, such as mites andnematodes. The number of susceptibleorganisms is expanding to include virtu-ally all invertebrate plant pests, as wellas insects that transmit human and animal pathogens. Key agricultural pestscurrently targeted with Bt insecticidesinclude bollworms, stem borers, bud-worms, and leafworms in field cropsand grains; the gypsy moth and spruce

budworm in forests; the cabbage looperand diamondback moth in vegetablecrops; and certain insects with chewingmouthparts such as beetles. While Btsprays are used on many crops, onlycotton, corn, and potatoes expressing BtICPs are commercially available. Mos-quitoes and blackflies targeted with Btsprays and aquatic treatments includethe blackfly vectors of Onchocercavolvulus, the etiologic agent of riverblindness; mosquito vectors of viralencephalitis and West Nile virus; andimmature forms of many nuisance mos-quito, blackfly, and midge species. Table1 gives a sample list of organisms thatare susceptible to Bt.

MECHANISMS OF ACTION AND RESISTANCEBt insecticides, whether in the form of aspray or a Bt crop, do not function oncontact as most chemical insecticidesdo, but rather, as midgut toxins. Theymust be ingested by the target organ-ism to be effective, and killing takeshours to days, longer than is required forsynthetic insecticides.

In the case of Bt sprays, parasporal crys-tals ingested by insect larvae feeding onplant surfaces dissolve and the insectici-dal proteins are activated by proteasesin the juices of the midgut, which typi-

FIGURE 3. ACTIVATION OF Bt ICP IN AN INSECT GUT. THE CONTENTS (BLUE BALLS) OF THE INSECT GUT EPITHELIAL CELLS ARE

SEPARATED FROM THE ALKALINE CONTENTS (YELLOW BALLS) OF THE GUT LUMEN BY THE CELL MEMBRANE. A. ICP IN THE

PRO-TOXIN FORM (RED SHAPE), ONCE DISSOLVED IN THE GUT LUMEN IS PROCESSED BY PROTEASE (YELLOW SHAPE) IN THE

GUT. B. THE TOXIN FORM OF THE ICP (RED SHAPE) BINDS TO SPECIFIC RECEPTORS (GREEN SHAPE) IN THE CELL MEMBRANE

AND INSERTS INTO THE MEMBRANE. C. SEVERAL ACTIVE ICPS (RED SHAPES) IN THE CELL MEMBRANE WILL COME TOGETHER,

FORMING A PORE. MIXING OF THE CONTENTS OF THE GUT LUMEN AND THE GUT EPITHELIAL CELL KILL THE CELL. THIS WILL

EVENTUALLY RUPTURE THE LINING OF THE GUT AND KILL THE INSECT.


ALFALFA CATERPILLAR

ALFALFA LOOPER

BAGWORM

BEET ARMYWORM

BLACK-HEADED FIREWORM

BLISTER BEETLE

BRUCE SPANWORM

BLUEBERRY SPANWORM

CABBAGE LOOPER

CITRUS CUTWORM

COLORADO POTATO BEETLE

CORN EARWORM

COTTON BOLLWORM

CRANBERRY FRUITWORM

CRANBERRY LEAFROLLER

DIAMONDBACK MOTH

EUROPEAN CORN BORER

FALL ARMYWORM

FALL CANKERWORM

FALL WEBWORM

FRUITTREE LEAFROLLER

FRUITWORM

FUNGUS GNAT

GRAPE LEAFFOLDER

GREEN FRUITWORM

GYPSY MOTH

HORNWORM

IMPORTED CABBAGE WORM

JAPANESE BEETLE

LEAFWORM

LINDEN LOOPER

OBLIQUE-BANDED

LEAFROLLER

OMNIVOROUS LEAFROLLER

PEACH TWIG BORER

PEAR CANKERWORM

REDHUMPED CATERPILLAR

SALTMARSH CATERPILLAR

SOD WEBWORM

SPINY LOOPER

SPRUCE BUDWORM

TENT CATERPILLAR

TOBACCO BUDWORM

TOMATO FRUITWORM

TWIG GIRDLER (MACADAMIA)

WESTERN GRAPELEAF

SKELETONIZER

WESTERN TUSSOCK MOTH

WESTERN YELLOWSTRIPED

ARMY WORM

TABLE 1. SOME AGRICULTURAL AND FORESTRY PESTS CON-

TROLLED BY Bt SPRAYS

Current Uses of Bt

SpraysViable bacterial spores constitute theactive ingredient in Bt spray formula-tions. Cry and Cyt ICPs are the primarycause of insect death. However, othercomponents in sprayed Bt pesticidescan contribute, especially in insectsthat are not very sensitive to Cry pro-teins. For example, the Bt spore isimportant to lethality to both gypsymoth larvae and to such pests as thebeet armyworm and the cotton boll-worm. The Bt spore germinates afterthe gut is damaged and then beginsvegetative growth, producing otherinsecticidal toxins and synergists. Theseinclude vegetative insecticidal proteins(VIPs), β-exotoxin, zwittermicin A, chiti-nases, and phospholipases.

Bt sprays comprise one to two percentof the global insecticide spray market,estimated to be U.S. $8 billion perannum. At one time, Bt sprays consti-tuted $100 million in annual sales, butwith the advent of transgenic plantsengineered with ICP genes, sales havedecreased to $40 million. Half of currentsales are used in Canadian forests tocontrol gypsy moths, spruce budworm,and other lepidopteran pests.

Bt sprays are used sporadically and typi-cally over small areas. In tropical andsubtropical areas (e.g., Hawaii), popula-tions of diamondback moth havebecome resistant to Bt sprays followingtheir intensive use. Crops sprayed withtraditional Bt formulations include vari-ous vegetables, tree fruits, artichokesand berries. Sprays are chosen byorganic farmers to meet guidelines forusing strictly non-synthetic materials.An additional use of Bt is in the protec-tion of stored commodities (e.g., wheat)from pest infestation.

Stability, persistence, and uniformity ofcoverage are major factors in determin-ing the probability that insects willdevelop resistance to Bt. When appliedas a spray, Bt is relatively unstable; itcan be washed off by rain or brokendown by ultraviolet light and may needto be reapplied as frequently as everytwo to four days. This instability, alongwith variable, low-dosage residues onthe plant may contribute to the emer-gence of resistant insect populations.These problems are avoided by higherand more uniform doses that can beobtained in Bt plants. In soil, the stabil-ity of ICPs is affected by microbialdegradation. In general, the drier thesoil, the longer an ICP will be stable, asthere is less microbial degradation.

cally are akaline (pH 8-10.5). In Bt crops,the plant tissues produce specific ICPsin a soluble form. In either case, theactive ICP then traverses the peritrophicmembrane and binds to specific recep-tors on the midgut epithelium, formingpores and leading to loss of the trans-membrane potential, cell lysis, leakageof the midgut contents, paralysis, anddeath of the insect. ICP activation andpore formation is shown in Figure 3. Onelevel of specificity in this interaction isprovided by the midgut environment ofthe insect, and a second by the bindingof ICPs only to membranes carrying theappropriately matched receptors.Insects that develop resistance to Btmost commonly exhibit decreased oraltered receptor binding, althoughaltered proteolytic activation also hasbeen reported.




Transgenic plantsApproximately 12 million hectares ofinsect-protected transgenic crops incor-porating Bt ICPs are now planted annual-ly worldwide. The vast majority of thesecrops are grown in the United States.Their total acreage has increased tenfoldsince 1996 and is expected to continueto increase along with other transgeniccrops. In 2001 the number of farmersplanting genetically engineered crops isexpected to have exceeded 5 million,and global areas planted in transgeniccrops are expected to have increased by10% or more since 2000. In March of2002, the Indian government announcedthat it would join the ranks of nationsallowing commercial use of geneticallyengineered crops by licensing Bt cotton.

Bt crops currently are engineered toproduce a single ICP continuouslythroughout all parts of the plant. TheICP gene is placed under the regula-tion of a promoter that is highly activein plants, and engineered so thatcodon preference is optimized forexpression in plants. The most widelydeployed transgenic crops expressingBt ICP genes are Bt corn, which isgrown in the U.S., China, Argentina,Canada, South Africa, Spain, Germany,and France; and Bt cotton, grown inthe U.S., China, Australia, Argentina,South Africa, and Mexico. Many addi-tional Bt crops are close to release,including rice, canola, and various veg-etables and fruits.

Evaluation of Bt Technologies

Comparing Bt sprays and transgenic cropsThere are advantages and disadvantagesto the use of Bt in spray form. Likechemical pesticides, the timing, dosage,and formulation of the application can be

controlled in any growing season tomeet specific pest pressures. The draw-backs are that spray can drift duringapplication, cannot be applied uniformlyto all parts of the plant, and cannot bedelivered to pests that are inside planttissues. Further, insecticidal crystals andspores of Bt exposed on plant surfacesare highly sensitive to degradation by UVlight and removal by water runoff. Multi-ple applications are therefore required toprovide extended pest protection.

Bt transgenic crops also have strengthsand weaknesses. ICPs are present athigh concentrations in most or all tis-sues in current transgenic plants. Thisfeature eliminates difficulties in targetingpests that burrow into plant tissues, aswell as the labor and expenses associ-ated with applying sprays. A potentiallimitation of engineered plants is thatthe ICP specificity cannot be changedwithin a growing season if resistancebegins to develop. Engineered plantsalso currently lack the componentsfound in bacterial formulations that actsynergistically with the ICP to kill par-tially resistant insects. In the event thata sexually compatible relative is near acultivated Bt crop, the risk that the Bttransgene could be transferred via pollenalso is an issue of concern.

Differences between Bt andother pest control methodsBt technologies—sprays or transgenicplants—will not control all insect pests.As with any pesticide, the potentialexists for target insects to developresistance. Both Bt sprays and Bt cropscan only harm close relatives of the target pest, and only if eaten. The pri-mary alternatives to Bt insecticides aresynthetic chemical pesticides withmuch broader toxicity, impacting manynon-target organisms including benefi-cial insects, fish, birds, and humanbeings. In the future, existing chemicalpesticides, as well as new chemicalscoming to market, will continue to pro-

vide alternatives to Bt. Although regis-tered based on extensive safety testing,these chemicals are viewed as beingless environmentally benign than Btmicrobial insecticides and Bt crops.

Farm workers have benefited from theuse of Bt sprays and Bt plants in place ofhazardous insecticides. The high speci-ficity of Bt ICPs not only leaves humansand other animals unaffected, but alsomakes these proteins harmless to thewide array of insects outside of their tar-get range. A testament to its safety isthat Bt is the only insecticide for whichthere are no mandated tolerance limitsfor residue in food. Bt transgenic plantsmore frequently displace syntheticinsecticides than Bt sprays. Both uses ofBt can contribute to agriculture.

Insect pest management strategies thatare available to agriculture need not beconsidered strictly as alternatives to Bt.Biocontrol through insect parasitoids orfungal pathogens, mating disruption,crop rotation, adjustments in date ofplanting, polyculture, and conventionalchemical sprays are all compatible withBt use. In particular, indigenous insectpopulations and introduced biocontrolagents that are harmed by broad spec-trum chemical pesticides are notgenerally harmed by Bt. Thus, Bt is well-suited to Integrated Pest Managementprograms that preserve large segmentsof indigenous invertebrate predator andparasitoid populations.

Bt crops can significantly reduce the useof synthetic insecticides and are highlycost-effective in controlling economi-cally important pests compared toexisting insecticides. Bt crops provideease of management by reducing theneed for repeated pesticide applications,the labor costs for scouting to deter-mine when to spray, the energy andequipment costs for applications, andthe danger of pesticide exposure to farmworkers. Conventional cotton is the


mental impacts of Bt on related nontar-get organisms or their predators.Because chemical insecticides are gen-erally used less frequently on Bt crops, itis likely that such crops will benefit non-target populations, especially those ofparasitoids and predators that controlinsect pests. In fact, studies in the U.S.,China, and elsewhere have documentedlarger populations of predatory bugs,spiders, and ants, and enhanced biodi-versity of beneficial insects in Bt cottonfields as compared with conventionalfields treated with chemical insecti-cides. Similar results have beenreported in Bt versus sprayed conven-tional potato fields. Studies examiningthe impact of Bt formulations in aquaticenvironments have failed to showadverse effects. Similarly, field studiesof forest applications of Bt sprays haveshown that the impact is restricted tomoths and butterflies and appears to betransient for many non-target organ-isms. Laboratory tests also have failedto show toxicity of Bt to birds, fish, andinvertebrates, including earthworms.

logical and health concerns. However, Btcorn that targets both corn borer andcorn rootworm will eliminate these risksto farm workers and the environment.

Impacts on Non-target OrganismsBt has a long history of use in spray formulations and is generally considereda safe insecticide because it is highlyspecific. It directly affects only targetorganisms and closely related species,although the biotic community may beaffected indirectly because of perturba-tions in insect populations. Populationsof non-target insect species belonging tothe same order as the target pest maybe vulnerable. Initial concerns about thenegative effects of pollen from Bt corn onthe larvae of the monarch butterfly,Danaus plexippus, have been allayed byadditional laboratory and field studies.

Field studies of transgenic crops havefailed to demonstrate significant detri-

most pesticide-intensive crop in theU.S., requiring upwards of 10 treat-ments per season. In Arizona, thedeployment of Bt cotton has reducedchemical insecticide applications from12 or 14 treatments to 2 to 6 treat-ments per season, with the number ofapplications depending on the growingregion and the season. In 1999, Bt cot-ton in the U.S. resulted in a reduction of1,200 metric tons of active ingredient ofinsecticides, and in China, a reduction of15,000 tons of formulated insecticide.From 1996 to 2000, U.S. farmers havesaved $100 million annually whenreduced pesticide costs and increasedyields are weighed against the addedpurchase cost of Bt cottonseed. A fur-ther benefit of Bt crops is reduction ofcertain food-contaminating toxins suchas the fungal toxin fumonisin in corn.

EnvironmentalConsiderationsDespite concerns about the use of Btsprays and Bt transgenic crops, bothtechnologies have advantages overstandard chemical insecticides. Unlikesome insecticides that accumulate inbiological systems, there are no datathat Bt proteins do so. Bt sprays and Btcrops only kill the target pests and someclosely related species, and only afteringestion of the Bt spray or plant. Bt cot-ton that targets the budworm andbollworm kills only these pests andrelated Lepidoptera when the plant iseaten. Bt corn is currently under devel-opment to control both the Europeancorn borer and the corn rootworm. Cornrootworm costs growers sums in excessof $2 billion annually in crop losses andinsecticide expenditures. Most chemicalinsecticides have a relatively broadrange of activity against nontargetorganisms including spiders, insect para-sitoids and predators, as well as fish,birds, and humans. Lorsban®, now usedto control corn rootworm, is broadlytoxic to invertebrates and presents eco-


The Monarch Butterfly, An Issue?

Non-target insects closely related to a targeted pest can be affected by ingestionof ICPs. However, the risk that any pesticide will affect a non-target organismdepends on both the dose that is toxic and the probability that the organism willbe exposed to that dose in its natural environment.

A controversial laboratory study raised concern about the impact of Bt on themonarch butterfly because monarch caterpillars were found to experience 44%mortality following ingestion of milkweed dusted with transgenic corn pollen.However, the levels of ICPs or pollen ingested in that study were not quantified,and the study did not address the probability that monarchs would be exposed totoxic doses of pollen containing ICPs in the field.

More recent assessments indicate that the actual risk to monarchs is negligible.These studies took into account the toxicity of Bt to monarchs in laboratory andfield studies, the amount and distribution of corn pollen on milkweed plants, andthe temporal and spatial overlap between patterns of monarch larval feeding andpollen shed from Bt corn. Although monarch larvae may experience less than 2%mortality by ingesting pollen from Event 176 Bt corn, other varieties produced nodetectable harm. This variety, a minor proportion of commercial plantings, is nowbeing withdrawn from the US market. In contrast, the studies showed that thewidely used corn insecticide, lambda cyhalothrin, has an adverse effect onmonarch butterflies. While research on potential long-term impacts of Bt pollen onmonarchs is ongoing, the experience to date illustrates that laboratory studiesalone cannot adequately evaluate the impact of a new technology at the field level.



Toxicity tests on a standard set oforganisms including avian and aquaticspecies, beneficial insects, soil inverte-brates, and mammals are requiredbefore pesticide registration, providing abasis for assessing potential toxicity tonon-target species. Fact sheets summa-rizing results from the testing ofcommercial Bt crops can be found at:www.epa.gov/pesticides/biopesticides/factsheets.

Laboratory and field tests can provideinformation about an organism’s suscep-tibility to Bt, the dose of Bt that is toxic,and the fate of Bt in the environment.However, these tests say little about therisks to non-target organisms. Riskassessment measures both the degreeof toxicity and the level of exposure andattempts to determine what effects Btwill have on a population under the conditions in which exposure will occur.For example, Bt sprays affect some non-target lepidopterans in the laboratory,but often the time of spraying does notcoincide with the presence of suscepti-ble non-target species, reducing theirexposure to Bt in the field.

Bt crops have only recently beendeployed and until now relatively smallsample sizes have been used in labora-tory and field studies. Thus the data insupport of the safety of Bt crops to non-target organisms is still limited.However, additional data are rapidlyaccumulating from field programs moni-toring the actual impact of Bt use onecosystems. Studies using large samplesizes of non-target organisms are under-way to determine the potential of bothshort- and long-term effects of Bt crops.Initial results have failed to reveal signifi-cant non-target effects, in contrast touse of standard chemical pesticides.

Will soil-dwelling non-target organismsbe affected by Bt ICPs? Laboratory stud-ies have shown that actively growing Btplants can increase the levels of ICPs insoil, and that soil can bind active Bt pro-teins for extended periods of time.However, there are no known toxicologi-cal effects of Bt ICPs on nontarget soilinvertebrates or microbes. Root exu-dates from transgenic Bt corn appear tobe nontoxic to earthworms, nematodes,

protozoa, fungi, and bacteria. BecauseBt is a natural inhabitant of soil, we alsoknow that soil organisms have a longevolutionary association with Bt.

Resistance in Target PestsInsects have the potential to developresistance to insecticides. Based on laboratory selection experiments and models derived from these studies, thepotential exists for development of resis-tance to Bt ICPs when these productsare overused or used incorrectly. Severalstrategies are available for resistancemanagement to Bt in spray formulations.These include the use of nontreatedrefuges, high dosage, mixtures of insec-ticidal toxins, and rotation or alternationof Bt toxins. After 40 years of use thereis only one known example (the dia-mondback moth) of control failure due toresistance to Bt sprays having developedunder field conditions, although otherspecies have developed high levels ofresistance through laboratory selections.

Because ICPs expressed in plants willsee increasing use, concern that insectpopulations will develop resistance isjustified. It is anticipated that resistancecould arise if management strategiesare not carefully followed, especially incrops based on single-gene technology.As with conventional pesticides, theevolution of resistance to ICPs willdepend on the genetics of resistance,the competitiveness of resistant individ-uals in the field, and the implementationof resistance management strategies.

The resistance management programpracticed most frequently for commer-cialized Bt crops is the “high dose/structured refuge strategy,“ in which thecrop produces an ICP at concentrationswith a goal of more than 99.9% lethalityin the target pest. High ICP concentra-tions in the tissues on which insectsfeed serve to counter incremental devel-opment of resistance. At the same time,from five to 50 percent (5-50%),

Measuring Effects on Non-target Organisms

Two main approaches are used to predict the impact of Bt on susceptiblenon-target organisms:

■ Toxicity tests conducted in the laboratory and field determine what dosesof Bt cause lethal or sublethal effects on representative non-target organ-isms. Ideally, field studies to quantify exposure are combined with feed-ing studies to determine if there is relevant exposure. The species thatrequire attention are those related to the target pest, close relatives ofendangered species, and beneficial species indigenous to habitatswhere exposure may occur.

■ Species diversity and abundance in a biotic community are measuredand compared to communities within similar agricultural lands. Analysesshould detect a negative or positive impact of Bt sprays or transgenicplants on biodiversity.

In either case, exposure studies should take into account persistence of theICP in the environment, direct and indirect exposure (food chain effects).Both short-term and long-term population effects should be considered.Finally, the impact of the spray or transgenic crop must be considered inlight of alternative pest control measures in a cost/benefit analysis.


Gene flow of Bt ICP genes from Bt cropsto wild relatives could occur where sex-ually compatible wild relatives are withinthe pollination range of the crop. Ecolog-ical consequences could result if thegene confers resistance to a pest that isa significant challenge to the wild rela-tive. This might provide a selectiveadvantage to the hybrid and its progenythrough introgression of the gene intothe wild relative’s gene pool. Negativeecological impact—predicted on acase-by-case basis—should beweighed against impacts of theaccepted alternative practices to Bttechnology, such as use of conventionalpesticides. In the U.S., the EPA has con-cluded that there is not a reasonablepossibility of gene flow from Bt cotton,corn, or potatoes to wild relativesexcept in certain areas of Florida andHawaii, where the use of cotton isrestricted because of the presence ofrelated wild species. There is a need forsimilar regulation globally, particularly incenters of crop origin, to insure that Btcrops are not grown in areas where

very low frequency. The probability thatsuch transfers will occur in nature, andinvolve functional genes is even lower.There is no evidence that genes fromnon-engineered crops have been trans-ferred to microorganisms and there isno basis to suggest that transgeneswould transfer more readily than anyother genes. Microbes are so muchmore likely to obtain genes, such asthose for antibiotic resistance, fromother microbes in the environment thatthe probability for such genes to beacquired from genetically engineeredplant DNA is insignificant.

Gene transfer between closely relatedspecies of plants occurs via pollenunder natural conditions all the time.Hybrids of conventional crops and wildrelatives form in 12 of the 13 most com-mon crops worldwide in some part oftheir agricultural range, and this processhas been implicated in enhanced weedi-ness about half of the time.

depending on the crop, of the acreage isplanted with a conventional version ofthe crop as a refuge for target insects.These conventional plants serve to sus-tain susceptible alleles within the insectpopulation. Through random mating,rare recessive resistance genes arediluted out of the insect population andprevented from providing a selectiveadvantage in offspring of the matings.This strategy will not be effective if casesdevelop where resistance is dominant.

Numerous studies have indicated thatseparate refuges are superior to seedmixtures in delaying the development ofresistance in insects that can movebetween plants in the larval stage. Caremust be taken in managing the insectpopulation within the refuge to ensurethat enough susceptible individuals willexist to breed out resistant individuals.The effectiveness of a refuge dependson consistent, appropriate implementa-tion and monitoring. Grower complianceto a resistance management strategy isessential to delaying the developmentof resistance. Similarly, proper applica-tion of Bt sprays would help to defer thedevelopment of resistance resultingfrom overuse, but presently only Btcrops have mandated resistance man-agement strategies.

New Bt crops that express multiple ICPswith different modes of action are currently being developed in a ‘genestacking’ strategy. This technique shouldlimit selection for resistance in targetand secondary pest species because theprobability of multiple, rare resistancemechanisms arising simultaneously isastronomically low.

Gene Flow to Other OrganismsAlthough it is theoretically possible formicroorganisms to incorporate DNAfrom transgenic plants, this has onlybeen accomplished under specificallyoptimized laboratory conditions and at a


TABLE 2.

BARRIERS TO GENE FLOW THROUGH POLLEN EXAMPLE/EXPLANATION

PHYSICAL BARRIERS

PLACEMENT OF BARRIERS TO POLLEN SPREAD . . . . . . . . . . . . . . . . . . . .PLANT NON-ENGINEERED BORDERS

RESTRICT LOCATION OR TIMING OF CROP PLANTING . . . . . . . . . . . . . . . . .PROHIBIT USE NEAR WILD RELATIVES

CONTAINMENT OF ENGINEERED CROPS . . . . . . . . . . . . . . . . .GROW CROPS IN GREENHOUSES

PHYSIOLOGICAL BARRIERS

HARVEST ENGINEERED PLANTS BEFORE FLOWERING . . . . . . . . . . . . . . . . .ONIONS, SUGAR BEETS

ENGINEER TRAITS INTO PLANTS THAT SELF-POLLINATE . . . . . . . . . . . . . . . .POTATOES, TOMATOES

ENGINEER TRAITS INTO PLANTS THAT ARE STERILE . . . . . . . . . . . . . . . . . .BANANAS

MAKE THE ENGINEERED PLANTS STERILE . . . . . . . . . . . . . . . . . . . .“TERMINATOR TECHNOLOGY”

PERFORM GENETIC MODIFICATIONS ON PLASTIDS . . . . . . . . . . . . . . . . . . . . . . .PLASTIDS ARE NOT IN POLLEN



potential outcrossing with wild orweedy relatives could introduce traitsthat might disturb biodiversity of culti-vated crop species. Any gene flow thatmakes a weed more competitive in thewild will not be readily reversed in theway that use of some short-lived envi-ronmentally damaging chemical can behalted. There are a wide variety ofmethods to limit gene flow betweenrelated plant species (Table 2).

Human HealthConsiderationsIssues have been raised regarding con-sumer and worker safety of Bt use,whether applied as a foliar spray orexpressed in plants. Food safety issuesinvolve the potential toxicity and aller-genicity of proteins, changes in thenutritional composition of plants, andthe safety of the antibiotic resistancemarker genes used during the processof genetic engineering. These issues arereviewed in a recent joint FAO/WHOpublication. Bt proteins in all Bt plantsand sprays registered for food consump-tion break down rapidly in simulateddigestive systems, do not resemble anyknown food allergen or protein toxin andhave no oral toxicity, even when admin-istered in high doses.

In some cases, Bt crops can improvefood safety. For example, approximately59% of corn grain globally is contami-nated with fumonisins, fungal toxinsproduced by the genus Fusarium thatcan cause liver and kidney damage inmany species, and are probable humancarcinogens. These fungal pathogensenter the plant through wounds causedby boring insects that are among themost important insect pests of cornworldwide. Bt corn is protected againstdamage from corn borers and consis-tently has 90% less fumonisin thanconventional plants. Thus, protectionagainst insect damage and subsequentfungal infection may have importanthealth implications for consumers andfarm animals exposed to fumonisins intheir diet.

Bt sprays and transgenic crops have nothad any known significant harmfuleffects on vertebrates, including mam-mals and human beings. There havebeen only a few reports of Bt bacteriabeing isolated from humans withwounds or infections, and in these rarecases there is no evidence that Bt wasthe cause of any lasting injury. It also

has been shown that farm workers donot develop respiratory, cutaneous, oreye diseases from exposure to largeamounts of Bt in sprays. They dodevelop antibodies to ICPs, but in nocase has the presence of these antibod-ies been linked to acute or chronicdisease. Thus, the use of Bt as a biologi-cal pesticide has proven to beremarkably safe for vertebrates, particu-larly in comparison with syntheticchemical insecticides. The health bene-fits to farm workers are clearlyillustrated in a recent report indicatingthat farmers in China currently growingBt cotton applied 80% less toxic insecti-cides than those growing conventionalcotton varieties. The farmers growing Btcotton also reported more than four-foldfewer instances of symptoms, such asheadache, nausea, skin pain, or diges-tive problems from applying pesticides.Bt cotton is the GE crop most frequentlyplanted by small farmers worldwide.Small farmers in developing countriesare at particular risk of exposure to pes-ticides because they often applypesticides by hand, without safety pre-cautions, such as respirators, goggles,and gloves.

For the Future

Improving our knowledgeWhile transgenic crops are beingadopted at unprecedented rates inlarge- and small-scale farming systemsworldwide, the technology remains con-troversial. Debate has arisen onimplications ranging from user, con-sumer, and environmental safety toglobal economics and world hunger.Many of the short- and long-term impli-cations have been predicted based onpast and ongoing experience, but muchremains to be learned because the tech-nology is new. Continued collaboration istherefore needed among scientists inacademia, government, environmentalgroups, and industry to critically define,

The StarLink® StoryLike other varieties of Bt corn, StarLink® produces an ICP that confersresistance to important insect pests, such as the European corn borer.However, StarLink® is the only Bt corn variety producing a particular ICPknown as Cry9C. At the time of its commercial launch, StarLink® hadbeen approved for use in animal feed only and not in foods for humanconsumption. In September of 2000 StarLink® corn was detected in TacoBell tortillas, prompting a rapid response that resulted in the voluntaryrecall of all StarLink® corn food products. The Scientific Advisory Panel ofthe EPA subsequently reevaluated the latest information available andconcluded that while no known health effects were associated withStarLink®, it did not meet the most stringent standards to rule out anypossibility of allergenicity. The product is no longer marketed and regis-tration has been withdrawn. The EPA estimates that StarLink® corn will be essentially eliminated from US grain supplies in 2002(http://www.epa.gov/oppbppd1/biopesticides/index.htm).


ble impacts on important soil organisms.Additional information also is needed onthe frequency with which pollen from Btcrops may fertilize other plants. In manycases, long-term environmental impactstudies were not possible before Btcrops were commercialized because ofthe scale and duration over which moni-toring is required. Agricultural systemsare disruptive to the environment, so itis imperative that these effects beclearly distinguished from those specifi-cally associated with Bt formulationsand genetically engineered plants.

Research should continue to generateand evaluate Bt engineered crops thatwill benefit developing nations, such asthe work being done by the InternationalRice Research Institute. Important con-tributions will also come from otherinternational centers of the ConsultativeGroup on International AgriculturalResearch that focus on wheat, corn, andpotatoes. This research is enhanced bycollaborations among scientists in acad-emic, government, and internationalresearch foundation laboratories in both

are not required for foliar sprays of Bt orother insecticides With increasingdeployment of Bt crops, it is important todevelop more sophisticated and reliableresistance monitoring and managementstrategies if sustained benefits are to begained from Bt technology. The potentialfor resistance development in target andnontarget organisms needs to be betterunderstood. What are the frequencies ofresistance alleles and what are the bestways to detect them? Are they domi-nant, recessive, or polygenic? What arethe mechanisms of action of ICPs at themolecular level and how do they influ-ence target insect specificity andresistance? Do ICPs delivered in spraysand plants differ in their effects on specificity and resistance? Will increased deployment of Bt crops influ-ence the rate of emergence of insectpopulations resistant to Bt sprays?

The need remains for a wide range offield studies to enable rigorous quantita-tive assessments of the direct andindirect effects of Bt sprays and cropson natural enemies and non-targetorganisms, especially as compared withtreatments that include standard pesti-cide controls. Longer-term and morecomplex studies should evaluate possi-

assess, and compare the risks and ben-efits of Bt sprays and crops relative toeach other and to conventional pestcontrol strategies. Scientific analysesshould monitor actual on-farm practices,include conventional laboratory and fieldstudies, and cover environmental im-pacts, effects on nontarget organismsand consumer safety. A thorough andobjective evaluation of known and unre-solved safety issues is essential toappropriate regulation of transgeniccrops in relation to the security, sustain-ability, and economics of foodproduction both on a regional scale andglobally. The eventual worldwideacceptance of genetic engineering willdepend not only on safety but alsodiverse cultural and societal norms.

With regard to Bt plants and formula-tions, many fundamental questions stillrequire answers. For example, what isthe baseline natural abundance and dis-tribution of B. thuringiensis in theenvironment? When we breathe, howmany Bt spores do we inhale? Howmany spores and crystals are consumedwhen we eat uncooked vegetables ororganically grown crops sprayed withBt? How does this compare with theamounts of ICPs ingested with Bt crops,and what is the relevance to consumerhealth? What factors influence thestability of insecticidal crystals andproteins introduced into soil in theform of sprays and plant exudates andresidues, and under what conditionsmight persistence have biologicallysignificant consequences?

Resistance of a pest to any insecticide isa serious concern. The U.S. Environ-mental Protection Agency requiresspecific insect resistance managementprograms for Bt corn, cotton, and pota-toes, which include refugerequirements,annual resistance monitoring, and reme-dial action programs (http://www.epa.gov/pesticides/biopesticides/otherdocs/bt_brad2/4%20irm.pdf). These programs




developing and developed countries. Allphases of such projects—from designto field-testing and consideration ofenvironmental issues—benefit fromthese collaborations.

TechnologyGene expression technology will play acritical role in the improvement of Btproducts. ICP genes in transgenic plantscan be genetically engineered for opti-mal efficacy and risk management.Refined engineering of genes may soonenable tissue-specific or inducibleexpression such that ICP proteins aresynthesized only at sites in plantswhere insects are feeding.

For crops such as corn and cotton, inwhich the pollen does not inherit plas-tids, plastid transformation systemswould prevent the dissemination of Bttransgenes through pollen. This also pro-vides the opportunity to introduceunmodified bacterial genes instead ofsynthetic genes and high protein yieldscharacteristic of plastid expression sys-

tems. Expression also can be engi-neered very specifically in the bacteriaused in sprays by manipulating geneticelements that aid in synthesis of ICPs.

Protein engineering has the potential tomake a significant contribution to Btapplications and insect control. Forexample, based on the current under-standing of the structure and mode ofaction of ICPs, researchers have engi-neered proteins with increased toxicityto target insects. In the future, thesame techniques can be used to nar-row the host range, reducing theimpact on non-target insects or biologi-cal control agents by increasing thespecificity of pesticidal proteins.Genomic information of insects maysuggest additional ways to improve theefficacy and specificity with which ICPsinteract with their molecular targets. Toaugment the arsenal of insecticidal pro-teins, searches should continue for new

varieties of ICPs and other types ofinsecticides of microbial origin.

CommunicationColloquium participants believe the sci-entific community could do a great dealmore to encourage the expansion ofgovernment and university programsaimed at communicating to the generalpublic the risks and benefits of using Btinsecticides and Bt crops. Scientists canwork with their professional societies topresent a balanced view of the risks andbenefits of these new technologies. Thiscan be done through white paperreports like this one, forums at scientificmeetings, articles in newsletters, andbeing available to members of the pressand the public. This report is available onthe web site of the American Society forMicrobiology (http://www.asmusa.org/acasrc/aca1.htm)

It is essential to foster public under-standing that long-term environmentaleffects of Bt crops and products gener-ally cannot be studied until after theproducts have been commercialized.Prior to the registration of the first Btcrop in 1995, the EPA evaluated studiesof potential effects of Bt endotoxins inthe environment. Based on their find-ings, they approved the use of Bt cropsbut realized that additional knowledgewas needed over the longer term toassess the risks and benefits of thistechnology. Environmental effects can-not be conclusively studied in thelaboratory; they must be studied in thefield. This post-release analysis is essen-tially what is done to assess theenvironmental effects of traditional plantbreeding and agricultural practices. Thepublic should be reassured that the useand monitoring of transgenic crops con-tinues to be more rigorously regulatedby governmental agencies than anyother agricultural technology.

The positive aspects and the risks ofagricultural biotechnology should be


Communication■ Professional societies should help

coordinate the dialogue between theinternational scientific community,the press, and the public.

■ Scientists should participate in exist-ing statewide outreach programs(such as cooperative extension services) that can disseminate infor-mation about the technology to thepublic and farming communities.

■ A pamphlet for the public should bedeveloped presenting objective infor-mation about Bt technologies.

■ A web site on Bt should be devel-oped as an educational tool for thepublic.

■ An international database should be developed and maintained tocentralize information concerningrisk-benefit assessment issues asso-ciated with the global adoption ofnew technologies in agriculture.

Recommendations

Research■ Develop and maintain integrated

international databases on Bacillusthuringiensis and ICPs.

■ Continue support for culture collections of Bacillus thuringiensisisolates and strains of relatedspecies.

■ Continue investigations into the persistence of ICPs and possiblelong-term effects on nontargetorganisms and the environment.

■ Evaluate and implement improvedresistance management strategies.

■ Evaluate gene flow to relatives of crops and improve strategies tomanage it through cultural practicesand engineered properties includingthe incorporation of Bt genes intothe plastid genomes of engineeredcrop plants.

clearly communicated to the public andcompared with the benefits and risks ofalternative technologies. Evidence col-lected to date indicates that geneticengineering of crops is at least as safeas conventional means of generatingnew crops. Many of the benefits of Btcrops, such as decreased productioncosts, reduced environmental impact,and lowered levels of contaminants inthe food supply, are not easily recog-nized by the consumer. Alternativescenarios to the use of Bt crops shouldbe presented, and the local, national,and international consequences of thesescenarios should be considered in rela-tion to food security, human health, andthe environment.

Enhanced communication should bestrongly encouraged among universityand government researchers assessingthe environmental effects of Bt cropsworldwide. This is particularly importantbecause Bt crops are grown in a varietyof agroecosystems, the same insectsare often a problem in different coun-tries, and both insects and weedyspecies frequently span national bor-ders. An international clearinghouse anddatabase would facilitate informationexchange pertaining to risks of emer-gence of resistance, nontarget effects,and potential gene flow to weeds andcrops. In addition to its value to the sci-entific community, this centralized,science-based resource will help to buildpublic confidence in genetic engineeringby documenting the activities of ongoingresearch and monitoring programs.




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Zangerl, AR, D McKenna, CL Wraight, M Carrol, P Ficarello, R Warner, and MR Berenbaum. 2001. Effects of exposure to event 176 Bacillus thuringiensis pollen on monarch and black swallowtail caterpillars inder field conditions. Proc. Natl.Acad. Sci. USA 98:11908-11912.

Zhao, JZ, Y Li, HL Collins and AM Shelton. 2002. Examination of the F2 screen for rare resistance alleles to Bacillus thuringiensis toxins in the diamondback moth. J. Econ. Entomol. 95:14-21.

A more detailed bibliography for this report is available on line (http://www.asmusa.org).


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100 YEARS OF Bacillus thuringiensis - IPM Florida

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