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Study finds that benefits of Bt corn may not outweigh potential risks (July 11, 2001 – CropChoice news) – Iowa State University entymologist John Obrycki gave CropChoice his permission to run a study about Bt corn that he and his colleagues published in the magazine BioScience. Here it is.
May 2001 / Vol. 51 No. 5 * BioScience 353 Articles
Transgenic Insecticidal Corn:
ANALYSIS OF TRANSGENIC INSECTICIDAL
CORN DEVELOPED FOR LEPIDOPTERAN
PESTS REVEALS THAT THE POTENTIAL BENEFITS
OF CROP GENETIC ENGINEERING FOR
INSECT PEST MANAGEMENT MAY NOT
OUTWEIGH THE POTENTIAL ECOLOGICAL
AND ECONOMIC RISKS
Many researchers have hailed transgenic insecticidal
crops-plants modified to produce insecticidal proteins
derived from genes of the bacterium Bacillus thuringiensis
(Bt)-as the most important technological advancement
in insect pest management since the development of synthetic
insecticides (Vaeck et al. 1987, Koziel et al. 1993, Perlak et al.
1990, 1993). At least 18 transgenic insecticidal crops have
been field-tested in the United States, and three (corn, cotton,
and potato) have been widely planted (Andow and Hutchi-son
1998, Federici 1998, Gould 1998, USDA 1999). But as the
commercial availability of these crops has grown, so too has
controversy over how to assess and manage the risks posed by
this method of pest control.
The widespread planting of millions of hectares of transgenic
crops with high levels of insecticidal proteins raises
concerns that pest populations might develop resistance to Bt
toxins and that food webs might be disrupted (Gould 1998,
McGaughey et al. 1998, Marvier 2001). Indeed, the US Environmental
Protection Agency (EPA) requires industry to
maintain populations of susceptible (nonresistant) insect
pests to slow development of resistant populations. Nor are
concerns limited to the United States: Anxiety over the safety
of food and products derived from transgenic crops have
created tensions among international trading partners (Balter
1997, Butler and Reichhardt 1999, Masood 1999).
In this article we focus on transgenic insecticidal corn (Bt
corn) developed for selected lepidopteran species that feed on
above-ground portions of the corn plant. Over 2.8 million
hectares of Bt corn were planted in the United States in 1998,
limited only by seed availability (Andow and Hutchison
1998); an estimated 9.7 million hectares of Bt corn were
planted in 1999. Thus, although acreage declined to approximately
6.2 million hectares in 2000, Bt corn is now the most
common management tactic for the European corn borer, Os-trinia
nubilalis, throughout the corn-growing regions of the
United States.
The potential benefits of transgenic insecticidal corn include
savings in resources devoted to scouting for pest insects, reduced
applications of broad-spectrum insecticides, increased
or protected yields due to season-long control of O. nubilalis
(Rice and Pilcher 1998), protection of stored corn from lep-idopteran
insect pests (Giles et al. 2000), and lower mycotoxin
levels due to a reduction in fungal plant pathogens associated
with O. nubilalis feeding (Munkvold et al. 1997, 1999).
Balanced against these potential benefits are possible drawbacks.
Such disadvantages of genetically modified crops can,
in general, be grouped into three categories: (1) selection for
resistance among populations of the target pest, (2) exchange
of genetic material between the transgenic crop and related
plant species, and (3) Bt crops' impact on nontarget species.
The potential for O. nubilalis to develop resistance to toxins
in Bt corn has been discussed in several publications (Gould
1998, McGaughey et al. 1998, Huang et al. 1999). Although
the transfer of genetic material between Bt corn and its wild
relatives can be a concern (Snow and Palma 1997, Bergelson
et al. 1998, Traynor and Westwood 1999), the potential for that
transfer is limited to Mexico and Central America, where
the wild species are located (Galinat 1988).
The impact of Bt corn
on nontarget species
We focus in this article on the potential negative effects of Bt
corn on nontarget species-specifically, the impact on arthropods
and microorganisms associated with corn. Recent studies
documenting negative impacts indicate that nontarget
effects may be subtle and complex, and thus may be overlooked
in the risk assessment conducted during the registration
process for governmental approval of this transgenic
crop (Figure 1a). Indeed, we examined the Web sites of EPA
and APHIS (Animal Plant Health Inspection Service, US
Department of Agriculture) and found no indication that po-tential
ecological interactions had been analyzed during the
registration process for transgenic corn. In this article we
discuss those ecological effects on several trophic levels within
and outside cornfields. Among species that were not explicitly
considered in the registration process but that may be adversely
affected by Bt corn pollen is the monarch butterfly
(Danaus plexippus), which we use as a case study in this
article.
Predators and parasitoids
Because research has shown that microbial insecticide formulations
of Bt have some negative effects on natural enemy
species (Croft 1990, Laird et al. 1990, Glare and O'Callaghan
2000), it is important to determine the impact of Bt corn on
populations of insect predators and parasitoids in the corn
ecosystem. Numerous insect species attack the European
corn borer in North America, including several predatory
species with relatively broad host ranges and insect parasitoids
that are specific to O. nubilalis (Steffey et al. 1999).
Tr ansgenic corn affects natural enemies in several ways: The
enemy species may feed directly on corn tissues (e.g., pollen)
or on hosts that have fed on corn, or host populations may
be reduced (Hoy et al. 1998). Data submitted for governmental
registration of transgenic crops appear to focus primarily
on direct feeding on corn tissues (USEPA 1999).
Because several species of insects that attack the corn borer
also feed on corn pollen, researchers have examined the effects
of corn pollen on these species (Table 1). Direct consumption
of transgenic corn pollen by immature stages of
three predatory species commonly found in cornfields did not
affect development or survival (Pilcher et al. 1997a). The
mortality rate of nymphal stages of the predator Orius ma-jusculus
was much the same when fed a thrips species reared
on Bt corn as when the thrips were fed on non-Bt corn
(Zwahlen et al. 2000). However, increased mortality of
lacewing (Chrysoperla carnea) larvae was observed when the
larvae fed on an artificial diet containing Bt toxin or preyed
on corn borers or other lepidopteran larvae that had fed on
transgenic corn (Hilbeck et al. 1998a, 1998b, 1999). Indirect
negative effects on predators have not been documented in
the field; sampling from transgenic cornfields has not shown
declines in predator abundance (Orr and Landis 1997, Pilcher
1999). In one field study, higher numbers of predators were
observed in Bt cornfields (Table 1).
The potential trophic-level effects of Bt corn on vertebrate
predators also need to be considered in an ecological assessment
of this biotechnology (Figure 1b), because bats and
birds are known to prey on larvae and adults of several lepidopteran
corn pests. Feeding Bt toxin directly to bobwhite
quail for 14 days produced no evident effect on the quail
(USEPA 1999). We are not aware of any studies that have considered
the indirect effects on bird populations resulting
from declines in O. nubilalis densities after use of transgenic
corn.However, if Lepidoptera and their predators and parasitoids
are significantly reduced in Bt cornfields and adjacent
margins, we might expect the insect prey available for birds,
rodents, and amphibians to decrease (see Watkinson et al. 2000
for a simulation of the potential effects of herbicide-tolerant
crops on seed-eating birds). When Bt sprays were purposely
used to reduce caterpillar abundance in a forest, fewer black-throated
blue warbler nests were observed in sprayed areas
(Rodenhouse and Holmes 1992). In one of the four years in
Figure 1. (a) Assessment of the risks from Bt corn based
solely on toxicological studies that examine direct effects
of Bt toxins on potential nontarget organisms. (b) A
broader ecological assessment of nontarget effects of Bt
corn based on the dispersal of transgenic corn pollen and
potential trophic-level effects on natural enemies.
Insect herbivores
The foundation for regulation of transgenic Bt crops is based
on a history of relatively safe use of Bt sprays (Laird et al. 1990,
Miller 1998, Glare and O'Callaghan 2000). The rapid break-down
of Bt toxins in the environment reduces the effects on
nontarget organisms, although studies of the ecological interactions
of Bt insecticide sprays have documented some effects
on nontarget organisms. For example, Tyr ia jacobaeae,
a beneficial lepidopteran introduced into North America for
biological control of the weed tansy ragwort, has been found
in laboratory bioassays to have increased mortality of fourth
and fifth instars after feeding on tansy ragwort leaves dipped
in Bt (James et al. 1993). Bt sprays can affect nontarget Lepidoptera
for up to 30 days after spraying (Johnson et al.
1995), and Bt drift effects have been observed up to 3000 meters
from a spray site (Whaley et al. 1998). Furthermore, a reduction
in lepidopteran species richness was found 2 years after
forest plots were sprayed with Bt (Miller 1990).
Many species of Lepidoptera, both target and nontarget, are
likely to be directly susceptible to the Bt toxins produced by
transgenic corn hybrids. Because herbivores that feed on
corn plant tissue within the cornfield are considered target
pests, we consider nontarget herbivores to be those species that
may contact corn pollen on weedy plant species within fields
or on plants outside of fields. The lepidopteran species most
likely to be affected by Bt corn pollen can be determined by
examining their distribution and phenology (Losey et al.
2001).
Plant communities within range of corn pollen dispersal
will, to a large degree, determine which herbivore (and therefore
natural enemy) species are most likely to be present and
subject to the effects of Bt corn pollen. An initial list of non-target
lepidopteran species can be generated by cross-referencing
the species of plants likely to be found near corn with
the species of Lepidoptera that feed on these and related
plant species. Because many plant species in and around
cornfields are considered to be weeds, the makeup of these
plant communities is fairly well known. Unfortunately, what
knowledge is lacking for most of the plants associated with
corn is the proportion of their total distribution that is composed
of field edges and the species composition of the lepidopteran
fauna. Specialist herbivores that feed on plants
that grow exclusively near corn would be of particular interest.
These herbivore species may be more likely to be affected
by Bt corn pollen than are herbivores that feed on plants
growing in several habitats in addition to cornfield margins.
Once it has been determined which lepidopteran species
feed on plants within the shadow of corn pollen, the next step
is to determine which subset of those lepidopteran species are
feeding in the larval stage during the period that corn pollen
is shed. Individual cornfields shed pollen for 8 to 10 days between
late June and mid-August (the period varies with corn
hybrid and latitude). Thus, to encounter corn pollen, larvae
must be feeding during or after this period, while the corn
pollen is still on the host plant. Unfortunately, we do not
know how long pollen remains on plants adjacent to cornfields
or how long the Bt toxin remains active within corn pollen.
The final step in predicting which lepidopteran species
are likely to be affected is to determine the relative susceptibility
of each species to Bt toxins expressed in transgenic
corn pollen. Although the toxin in Bt corn is active against several
lepidopteran families, variation in susceptibility has been
observed (Pilcher et al. 1997b, Williams et al. 1997, 1998,
Wraight et al. 2000). It may be possible to link susceptibility
and phylogeny to allow prediction of susceptibility of a given
lepidopteran species. Integrating distribution, phenology,
and susceptibility permits a ranking of the risk to specific lepidopteran
species. Species at particularly high risk could then
be identified for further testing.
Case study: The monarch butterfly
The monarch butterfly, Danaus plexippus, is widely distributed
in North America, producing up to five generations in
the United States and Canada (Brower 1996). Several factors
may make the risk to monarch butterflies from Bt corn pollen
higher than risks to other nontarget lepidopteran species.
Monarchs migrate annually in spring and summer from
overwintering sites in Mexico to breeding areas across eastern
North America (Brower 1996). Fifty percent of the over-wintering
adults in Mexico originate from the central United
States, the major corn-growing area in North America (Wasse-naar
and Hobson 1998).
The common milkweed, Asclepias syriaca, is a secondary
successional plant that frequently occurs in and around the
edges of cornfields (Bhowmik 1994, Yenish et al. 1997, Hartz-ler
and Buhler 2000); it is the primary host plant of monarch
butterflies in the northern United States and southern Canada
(Malcolm et al. 1989), and monarch larvae feed exclusively on
milkweed leaves (Malcolm et al. 1993). Monarch females
oviposit on milkweeds throughout the summer; the egg laying
that gives rise to the fall migratory generation occurs
from approximately 20 July to 5 August in the northern half
of the corn belt. Corn anthesis, in which pollen is dispersed
at least 60 meters by the wind (Raynor et al. 1972), coincides
with this time period over large areas of the Midwest. Thus,
the monarch, milkweeds, and Bt-corn pollen overlap spatially
and temporally in the central United States.
A recent study has shown that monarch larvae reared for
96 hours in the laboratory on milkweed leaves dusted with
pollen from Bt corn suffered significantly higher mortality
(44%) within 96 hours than did larvae reared on leaves dusted
with untransformed corn pollen or leaves without pollen
(Losey et al. 1999). In addition, larvae that were fed leaves
dusted with pollen from Bt corn consumed significantly less
foliage per larva and grew significantly slower. In field studies,
transgenic corn pollen was naturally deposited on A. syriaca
leaves within and adjacent to a transgenic cornfield (Jesse
and Obrycki 2001). The levels of pollen deposition were
highest on plants within the cornfield and lowest 10 meters
from the field edge.
Leaf samples taken from within and at the edge of the
cornfield were used to assess mortality of first-instar D. plexippus.
Within 48 hours, mortality was 20% for those instars
exposed to Bt-corn pollen, compared with 0% for those not
exposed to Bt-corn pollen and 3% for controls not exposed
to any pollen (Jesse and Obrycki 2001 ). Mortality (at 120
hours) of D. plexippus larvae exposed to 135 pollen grains/cm 2
of transgenic pollen for 48 hours ranged from 60% to 70%
(Jesse and Obrycki 2001). No sublethal effects were observed
in adult D. plexippus reared from larvae that survived 48
hours of exposure to three concentrations of Bt corn pollen
(Jesse and Obrycki 2001).
Based on these laboratory and field results, it appears that
pollen from Bt corn may pose a risk to monarch populations.
Monarchs may also be negatively affected by the use of transgenic
corn and soybeans that are resistant to the herbicides
Roundup and Liberty. If these herbicides are used to kill
weeds in these transgenic crops, then the abundance of milk-weed,
which supports monarch populations in agricultural
fields, will decline (Taylor et al. 2000).
Pollinators
An assessment of the impact of each Bt-corn hybrid on pollinators
is required for EPA registration (USEPA 1999). Although
the toxins expressed in Bt-corn pollen are specific for
Lepidoptera, several studies raise questions about Bt effects
on pollinators, that is, domesticated and wild bees. Documentation
for the EPA registration shows that pollen from Bt
corn has no effect on survival of either larval or adult domesticated
bees (USEPA 1999). However, some unexpected
effects of transgenic plants on domesticated bees have been
reported. For example, one preparation of Bt (var. tenebrio-nis),
reported to be specific for Coleoptera, caused significant
mortality in domesticated bees (Vandenberg 1990). Another
study indicated that proteins (other than Bt) produced in
transgenic rapeseed pollen and targeted for Coleoptera and
Lepidoptera interfered with learning by domesticated bees
(Picard-Nioi et al. 1997). These studies raise concerns about
the precision of genetic transformations and the unintended
side effects of genetic transfers. In addition, although wild bees
provide a substantial amount of the pollination in many systems,
they apparently were not tested for registration of Bt
corn.We are not aware of any studies that have examined the
impact of Bt pollen on wild bees.
Decomposers
According to the EPA, the insecticidal toxin (CryIA[b]) found
in one type of transgenic corn caused significant mortality and
reduced reproduction in the soil-dwelling collembolan Fol-somia
candida (USEPA 1999). An earlier study, however, had
shown no effects on F. candida from feeding on transgenic cotton
leaves, which contained the same insecticidal protein as
in the corn (Yu et al. 1997). The higher dose in the corn appears
to have caused the adverse effects.
Despite its own finding of an adverse effect on a nontarget
species, the EPA has concluded that there is a 200-fold
"safety factor" in the levels of toxin present in the field (USEPA
1999). The meaning of this EPA safety factor is not entirely
clear, though perhaps it signifies that the concentration of Bt
toxin in corn residue or soil is less than 1/200th of the concentration
needed to kill Collembola. In addition, because no
buildup of cornstalk residues has been observed after use of
soil insecticides in cornfields, which presumably would have
a negative effect on Collembola,"an observable deleterious effect
on the soil ecosystem is not expected to result from the
growing of CryIA(b)-endotoxin-containing corn plants"
(USEPA 1999). This conclusion may need to be rethought:
Considering the seasonal life cycle of Collembola, there are potentially
important differences between the use of soil insecticides
at planting and the occurrence of transgenic Bt toxins
in roots (Saxena et al. 1999), pollen deposition, and stalk
residues at harvest.
Microorganisms
We found no consideration of the interactions between transgenic
corn and plant pathogens or beneficial insect pathogens
in the EPA registration documentation for Bt-corn hybrids
(USEPA 1999). An ecological approach to evaluating the effects
of Bt corn would, we believe, greatly enhance the effectiveness
of the registration process in assessing the potential
nontarget effects of this new technology.
Tr ansgenic insecticidal corn reduces the incidence of plant
pathogens that infect corn following attack by O. nubilalis
(Munkvold et al. 1997). These plant pathogens also produce
mycotoxins, which may be harmful to humans and livestock;
levels of these compounds also were reduced in transgenic corn
(Munkvold et al. 1999). Reductions in mycotoxin levels were
observed when both Bt- and non-Bt-corn hybrids were artificially
infested with high densities of corn borer larvae. In two
of three field seasons, however, no differences in mycotoxin
levels were observed when relatively low densities of naturally
occurring O. nubilalis larvae infested the Bt and non-Bt plots
(Munkvold et al. 1999)
Two insect pathogen species infecting O. nubilalis in North
America are Nosema pyrausta,a microsporidum, and Beau-veria
bassiana, an entomopathogenic fungus (Steffey et al.
1999). Nosema pyrausta appears to be specific to the corn borer,
so we would expect declines in corn borer densities to affect
its prevalence. In contrast, the fungus B. bassiana may not be
adversely affected by transgenic corn because it attacks a
wide range of insects and forms a symbiotic relationship
with the corn plant (Bing and Lewis 1991).
Risk mitigation for Bt-corn pollen
We suggest three strategies for reducing risks for nontarget
species associated with pollen from Bt corn. The simplest
strategy would be to use only those Bt-corn hybrids that do
not express the Bt toxin in the pollen. Expression in pollen is
controlled by a single gene promoter (Fearing et al. 1997), and
there are commercial hybrids that do not express detectable
levels of Bt toxins in pollen (Andow and Hutchison 1998;
USEPA 1999). The drawback of this strategy is that Bt-corn
hybrids lacking Bt toxin in the pollen may not be as effective
against first-instar O. nubilalis,which feed on corn pollen before
feeding on plant tissues. This lower efficacy may present
problems for resistance-management programs that are based
on high mortality of target populations (Ostlie et al. 1997).
An alternative solution would be to create buffer zones of
non-Bt corn around Bt cornfields (Rice 1999). Very little
corn pollen travels more than three or four rows from the original
plant (Louette 1997). A buffer zone of at least four rows
would serve to trap most transgenic pollen. Some 20% to 30%
of the corn a grower plants should be nontransgenic, so that
it may serve as a refuge in resistance management (Ostlie et
al. 1997), which in turn might be used as a buffer zone for Bt
pollen collection. The size and shape of the areas of non-Bt
corn would have to be designed carefully to ensure that they
effectively serve both purposes.
Simply not planting transgenic corn hybrids, a third option,
would eliminate the potential risks to nontarget species that
this biotechnology poses.
Conclusions and recommendations
Unlike the use of transgenic potatoes and cotton, the use of
transgenic corn will not significantly reduce insecticide use in
most of the corn-growing areas of the Midwest. During the
past 5 years, the percentage of field corn treated with insecticides
in the United States has remained at approximately
30%, despite a significant increase in the hectares of Bt corn
planted (Figure 2). From 1995 to 1998, about 1% to 2% of the
corn grown in Iowa-where over 4 million hectares of corn
are grown annually-was treated with insecticides for O. nu-bilalis
(Figure 3). A survey of veteran corn farmers in Iowa and
Minnesota-the average farming career was 21 years-showed
that 70% had never used insecticides for the first generation
of the corn borer, and 82.7% had never treated for the second
generation (Rice and Ostlie 1997). Approximately 5% had used
insecticides three or more times in 21 years to manage the corn
borer.
Despite the relatively low use of insecticides during the
1990s for corn borer suppression, between 20% and 30% of
the corn planted in the United States in 1998 and 1999 was
transgenic (Fernandez-Cornejo and McBride 2000), suggesting
that the Bt plantings are not being used as a replacement
for insecticides but in addition to them. A core concept
of integrated pest management is to use a management tactic
only when pest populations exceed a threshold level. It
seems, then, that the hectares planted in Bt corn represent a
change in approach from management of O. nubilalis to a prophylactic
strategy.
Because population densities of the European corn borer
are unpredictable, the economic benefits of using transgenic
corn are not assured (Rice and Pilcher 1998, Hyde et al. 1999,
Archer et al. 2000). Comparisons of yields from transgenic and
genetically similar nontransgenic corn hybrids grown in replicated
plots in 14 to 16 locations in Iowa (Farnham and Pilcher
1998, Rice 1998) showed that only 34% of the transgenic
lines produced significantly higher yields in 1997. In locations
Figure 2. The percentage of field corn treated with
insecticides and the number of hectares of transgenic Bt corn
planted in the United States from 1995 to 1999. Insecticide
data from USDA Agricultural Chemical Usage, National
Agricultural Statistics Service for Field Corn. (1 May 2001;
usda.mannlib.cornell.edu/reports/nassr/other/pcu-bb/)
Figure 3. Percentage of field corn treated with insecticides in
Iowa, 1995 to 1998. Data from Howard Holden, Iowa
Agricultural Statistics, and Rich Pope, Iowa State University
Extension Service. In 1995, 2.2% of the field corn in Iowa was
treated with broad-spectrum insecticides for the European
corn (Wintersteen and Hartzler 1997). In this report, 31.3%
of the corn acres in Iowa were treated with insecticides
(Wintersteen and Hartzler 1997), similar to the 27% recorded
by the Iowa Department of Agriculture Statistics. We
calculated that about 7% of the treated acres of field corn
were sprayed with broad-spectrum insecticides for the corn
borer. Using this 7% value, we estimated the acres treated for
the corn borer for 1996 to 1998. It is quite likely that the
percentage of acres treated for the corn borer in 1995 did not
vary significantly from that found for 1996 to 1998.
--where corn borer damage was highest in nontransgenic lines,
50% to 58% of the transgenic hybrids produced significantly
higher yields. In 1998, when corn-borer densities were generally
lower than usual in Iowa, 12% of transgenic lines produced
significantly higher yields.
Further analysis of these comparative data shows a weak relationship
(r 2 = 0.13) between the amount of insect damage
and increased yields in the Bt corn in 1997 and no relationship
in 1998. Analysis of a second data set collected for the
USDA National Agricultural Statistics Survey in 1998 showed
no economic benefit of transgenic insecticidal corn in Iowa
(Duffy and Ernst 1999), probably because of differences in the
amount of fertilizer applied to the Bt and non-Bt fields. Previous
assessments of Bt corn have indicated that the economic
benefits of this technology are highly dependent on the
population densities of the corn borer and the market value
of field corn (Rice and Pilcher 1998). From 1997 to 1999, corn
borer densities were generally low in Iowa and the value of field
corn had declined. Thus, in these 3 years the economic benefits
of Bt corn were not consistently demonstrated.
Given the limited benefits for insect management and the
documented ecological effects of transgenic insecticidal corn
on nontarget species, we conclude that this biotechnology has
a limited role in management of lepidopteran pests in corn.
The use of transgenic crops has been promoted as safer for humans
and the environment than use of broad-spectrum insecticides
(Pimentel and Raven 2000). However, most field
corn in the US corn belt is not treated for above-ground insect
pests, and most corn hybrids already have substantial resistance
to corn borers (Barry and Darrah 1991).
The approach taken in the registration of transgenic corn
and in its current use in pest management has been narrowly
focused on insecticidal toxicity, but we believe that a
more comprehensive approach is required (see, e.g., Stern et
al. 1959, Lewis et al. 1997), one that considers the ecological
complexity of agroecosystems (Figure 1b). We have outlined
in this article the potential benefits and ecological risks of the
use of Bt corn. These potential risks are not thoroughly ad-dressed
in the US governmental registration process, an over-sight
that should be attended to.
The widespread and unquestioned acceptance of Bt corn
by the agricultural research, regulatory, and educational communities
is similar to the rapid adoption and deployment of
synthetic insecticides in the early 1950s. During that time, ecologically
based management programs suffered, and predicted
adverse ecological and environmental effects were
generally ignored, resulting in limited management options
for farmers as targeted species developed resistance and non-target
predator and parasitoid species declined. We are not advocating
the elimination of Bt corn, nor do we discount the
potential benefits of biotechnology for agriculture. We do argue,
however, that a balanced examination of Bt corn suggests
ways to improve the regulatory process and to incorporate this
technology into an integrated control framework, and we
caution against the acceptance of yet another silver bullet
for pest management.
Acknowledgments
We thank the following colleagues for their critical reviews of
this manuscript:
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May 2001 / Vol. 51 No. 5 * BioScience 359
Articles
John J. Obrycki (e-mail: jobrycki@iastate.edu) is a professor in the
Department of Entomology and chair of the Ecology and Evolutionary
Biology program, Iowa State University, Ames, IA 50011 Laura
C. H. Jesse, an EPA STAR (Science to Achieve Results) Fellow, also
works in the Department of Entomology at Iowa State. John E.
Losey is an assistant professor in the Department of Entomology at
Cornell University, Ithaca, NY 14853. Orley R. Taylor is a professor
in the Department of Entomology and in the Department of Ecology
and Evolutionary Biology at the University of Kansas, Lawrence, KS
66045. © 2001 American Institute of Biological Sciences.
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