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Date:

December 13, 2000

Subject:

The Ecological Risks and Benefits of Genetically Engineered

 

I reproduce here below a rather critical paper from the recent Science
journal (but without the tables or the figure). See also the New York
Times piece commenting on this work.

- Prakash
-------
The Ecological Risks and Benefits of Genetically Engineered Plants

L. L. Wolfenbarger 1 * and P. R. Phifer 2
ww.sciencemag.org SCIENCE VOL 290 15 DECEMBER 2000 2088093

(mail: wolfenbarger.lareesa@epa.gov)

Discussions of the environmental risks and benefits of adopting
genetically engineered organisms are highly polarized between pro and anti
biotechnology groups, but the current state of our knowledge is frequently
overlooked in this debate. A review of existing scientific literature
reveals that key experiments on both the environmental risks and benefits
are lacking. The complexity of ecological systems presents considerable
challenges for experiments to assess the risks and benefits and inevitable
uncertainties of genetically engineered plants. Collectively, existing
studies emphasize that these can vary spatially, temporally, and according
to the trait and cultivar modified.

Ecologists and other scientists have long expressed concerns about the
potential impacts of releasing genetically engineered organisms (GEOs)
into the environment (1), while others emphasize their potential
environmental benefits. The broad implications of national and
international regulations underscore the policy and research communities’
need for current scientific information and for awareness of where
informational gaps occur. Here, we synthesize available empirical,
published information, primarily from academic, peer-reviewed journals, on
the potential environmental risks and benefits of genetically engineered
plants. Our focus reflects a current emphasis on crop plants, but
developments of genetically engineered fish, trees, and microbes may alter
perspectives.


Potential Risks
Risk of invasiveness. The release of GEOs highlights the general
difficulty in predicting the occurrence and extent of longterm
environmental effects when nonnative organisms are introduced into
ecosystems. Nonindigenous species have been introduced into the United
States intentionally and unintentionally for centuries; an estimated
50,000 species in the United States are not native (2). While many
nonindigenous species are regarded as harmless or beneficial, other
introduced species, commonly referred to as invasive species, have spread
widely in their nonnative ecosystems and caused unintended degradation of
natural ecosystem functions and structure (2, 3). Invasive species are
also expensive, costing the United States an estimated $137 billion
annually in direct and indirect effects, and control or prevention
measures (2). Indeed, invasive species have been categorized as one of the
three most pressing environmental problems, in addition to global climate
change and habitat loss (4).

Genetic modifications, through traditional breeding or genetic
engineering, of crop or other species can potentially create changes that
enhance an organism’s ability to become an invasive species. Although
genetic engineering transfers only short sequences of DNA relative to a
plant’s entire genome, the resulting phenotype, which includes the
transgenic trait and possibly accompanying changes in traits, can produce
an organism novel to the existing network of ecological relationships.
Potential ecological impacts through invasiveness depend on existing
opportunities for unintended establishment, persistence, and gene flow of
an introduced organism; each of these, in turn, depends on various
components of survival and reproduction of an organism or its hybrids
(Fig. 1). Few introduced organisms become invasive, yet an issue for the
management of all introduced organisms, including GEOs, is how to identify
those modifications that may lead to or augment invasive characteristics.

For GEOs, one approach has compared the likelihood that transgenic
organisms or their hybrids would persist outside of cultivation compared
to non transgenic controls. Two experiments on oilseed rape suggest that
self sustaining populations were unlikely under these experimental
conditions (5–7) ( Table 1). In contrast, some evidence indicates that
under experimental conditions transgenic crops can hybridize with closely
related species or subspecies ( Table 1), a prerequisite for gene
introgression. Such results are not surprising. Natural hybridization
occurs between 12 of the world’s 13 most important food crops, including
wheat, rice, maize, soybean, barley, and cotton seed, as well as numerous
other crop species, and some wild relatives (8, 9). Large areas of
cultivation may increase the opportunity for range overlap with compatible
relatives; therefore, the probability that crop genes, newly introduced
through genetic engineering or through other, more traditional techniques,
will introgress into wild relatives may increase as particular cultivars
are more widely adopted. Genetic modifications could change the propensity
of outcrossing (10), although this has not been reported in the one crop
species studied (11).

Ecological impacts of pollen transfer, a reproductive mechanism through
which introgression might occur, depend on whether hybrids survive and
reproduce. Equivocal rates of survival or reproduction between transgenics
and controls suggest, but do not indicate, the opportunity for
introgression of transgenes into natural populations (12–17), depending on
subsequent gene flow and selective pressures. Not all studies support
these conclusions (18), and ecological consequences in nonagricultural
habitats and ecosystems largely remain unstudied.

No published studies have examined whether introgression of transgenes or
its potential ecological consequences have occurred in natural
populations; however, past experience with crop plants suggests that
negative effects are possible. For seven species (wheat, rice, soybean,
sorghum, millet, beans, and sunflower seeds) of the world’s top 13 crops,
hybridization with wild relatives has contributed to the evolution of some
weed species (8). In some cases, high levels of introgression from
cultivated or introduced relatives have eliminated genetic diversity and
the genetic uniqueness of native species, effectively contributing to
their extinction (8, 19, 20).

The complex nature of biological invasions means that simple comparisons
of fecundity and survival will not adequately predict invasiveness.
Variation in the competitive environment and timing of introductions can
confound predictions (21, 22). Unknown factors cause unexplained time lags
that occur between the establishment of an introduced species and the
subsequent expansion of its population and range (23). These represent key
challenges for assessing the risk of invasiveness. A thorough
understanding of factors, such as viral infections, insect predators,
competition, or human mediated controls, that limit reproduction will
highlight how transgenic traits affect the reproductive ability of GEOs
and their wild relatives in different ways so that we may consider what,
if any, ecological impacts might arise from any differences.

Direct nontarget effects on beneficial and native organisms.
Plants engineered to produce proteins with pesticidal properties, such as
Bacillus thuringiensis (Bt) toxin, may have both direct and indirect
effects on populations of non target species. One group of toxins from Bt
primarily targets Lepidoptera (butterflies and moths, such as the European
corn borer), and another mostly affects beetles (Coleoptera) (24). Effects
on non pest species in these groups could vary widely owing to differences
in sensitivity among species and concentration of Bt toxin produced by
tissue or by transgenic lines (25, 26). Laboratory experiments suggest
that adverse effects may occur when monarch butterfly larvae ingest Bt
corn pollen on host plants (25, 27). How broadly these results apply to
natural populations is not known because neither study addressed the rate
at which larvae encounter the toxin, a necessary component for assessing
risks. How these potential risks compare with those of chemical pest
control remains critical to understanding the net effect of Bt crops on
nontarget populations. In contrast, other studies show no direct effect of
transgenic Bt crops on nontarget organisms for particular life history or
reproductive traits measured (26, 28, 29).

Some genetically engineered crops affect soil ecosystems (30–34), but the
long term significance of any of these changes is unclear. At least two
consequences could potentially occur from reported alterations of soil
ecosystems—decrease of plant decomposition rates and of carbon and
nitrogen levels, which could affect soil fertility (35). Similarly,
declining species diversity of soil microorganisms, in some cases, can
cause lower community diversity and productivity above ground (36).

Indirect effects.
GEOs may have indirect impacts on populations of species that depend on
the pests controlled for survival or reproduction. Population models
suggest that more effective control of weeds by using herbicide tolerant
crops could lead to lower food availability for seed specialists (37).
Effective control of the Colorado potato beetle in trans genic fields
probably explains the decrease in a predatory specialist on it (38). In
contrast, population estimates of predatory insects were similar in plots
of Bt and nontransgenic corn (39).

Pesticidal proteins produced by GEOs may have effects indirectly through
bioaccumulation, if exposure occurs when predators consume prey items that
contain pesticidal proteins. When Bt spores are sprayed to control
insects, the toxins they contain rapidly decline in abundance and toxicity
(24), leaving little opportunity for bioaccumulation. In accordance, some
studies conducted with Bt crops indicate no effects on survivorship or
reproduction of predatory insects that eat prey items that have ingested
genetically engineered Bt plant tissue (40–42) ( Table 2). In contrast,
other studies suggest that the opportunity for bioaccumulation may occur
(43, 44) ( Table 2). Like most studies on direct effects, field exposure
levels to the toxin and toxin laden prey are unknown. Therefore, with the
data available from published, peer reviewed literature, extrapolation of
these results to natural ecosystems cannot yet be made.

The rate of persistence of pesticidal proteins may affect the probability
of nontarget effects. In neutral soil pH, bioassays revealed a rapid
decline in the biological activity of Bt toxin from transgenic cotton and
transgenic corn (45, 46), and at 120 days, the soil inhibited larval
growth by 17 to 23% of its starting biological activity (46). Similarly,
varying rates of persistence of Bt toxin from transgenic plant tissue,
from 0 to 35%, remained detectable through soil extractions after 140 days
(47). In soil, high microbial activity degrades Bt toxin, but active toxin
readily binds to soil particles, an association that inhibits
biodegradation (24). Purified, active Bt toxin persisted in certain soil
types for at least 234 days, the longest duration studied (48), and high
clay content and low soil pH increased the persistence (24). Information
on how prevalent these conditions are within agricultural systems and
nearby ecosystems will reveal the extent to which these data indicate a
risk.

Laboratory results suggest the possibility that Bt toxin may contact soil
ecosystems by way of exudate from Bt corn plant roots (49), but results
under field conditions have not been reported. Any ecological consequences
of the presence and persistence of Bt toxin in soils have not been
published, and empirical studies addressing these consequences will
provide much needed information to evaluate the possibility of long term
effects on non target organisms and how these compare to risks when
chemical pest control is used.

New viral diseases. Viruses with new biological characteristics could
potentially arise in transgenic viralresistant plants through
recombination and heteroencapsidation (50). New viral strains can evolve
through recombination between closely related strains, and transference of
transgenic sequences can occur under laboratory conditions (51, 52).
However, we lack empirical evidence to understand the likelihood of this
transference under natural circumstances. As occurs in other plant
viruses, closely related viruses can exchange coat proteins (CPs). Under
laboratory conditions, CPs produced by transgenic virus resistant plants
encapsidated a related virus that subsequently altered its
transmissibility (53). Again, we lack empirical data to understand the
prevalence of these events under more natural conditions. The modified,
encapsulated virus cannot produce the new CPs because its genome does not
contain those genes; therefore, new viral strains created through
heteroencapsidation are not propagated (50). Strategies to reduce the
biological risk of heteroencapsidation and accompanying changes in
transmissibility are under investigation (54.).

Variability and unexpected results. Ecosystems are complex, and not every
risk associated with the release of new organisms, including transgenics,
can be identified, much less considered. Unknown risks may surface as the
frequency and scale of the introduction increases (55). Because some
consequences, such as the probability of gene flow, are a function of the
spatial scale of the introduction (56), limited field experiments do not
always sufficiently mimic future reality prior to widespread planting.
Ecological relationships include many cascading and higher order
interactions that are intrinsically difficult to test and evaluate for
significance at limited temporal and spatial scales. At larger spatial
scales, there is a greater possi bility for contact with sensitive species
or habitats or for landscape level changes because at larger scales more
ecosystems could be altered (57).

Environmental and cultivar variability complicates the task of assessing
risk. Transgenic organisms, such as genetically engineered crops, released
into the environment will potentially interact with a diversity of
habitats in time and in space, and the potential risks from a single type
of transgenic organism may vary accordingly. For example, among cultivated
and natural populations, gene flow can occur regularly or not at all, and
substantial variation in risks from gene flow may arise from variation
among cultivars, from factors such as distance from the source population,
or from the size and density of the source population relative to
recipient populations. Risk assessments will need to be especially
sensitive to temporal and spatial factors.


Potential Benefits Reduced environmental impacts from pesticides. As
regulations are considered, the potential risks of GEOs should be
evaluated and compared to possible environmental benefits, as well as to
risks from conventional and other agricultural practices, such as organic
farming. Insectresistant and herbicid etolerant transgenic crops may
decrease the use of environmentally harmful chemicals to control pests. In
1998, 8.2 million fewer pounds of active pesticide ingredient (3.5%) were
used on corn, cotton, and soybeans than in 1997 and corresponded to an
increase in the adoption of genetically engineered crops (58). Annual
variation in agrochemical use can depend on multiple factors, including
pest problems, weather, and cropping patterns (59), besides adoption of
genetically engineered crops. Statistical models controlling for
additional factors influencing pesticide use estimated that the total
volume of pesticides used on corn, cotton, and soybeans in 1998 decreased
2.5 million pounds (1%) owing to the adoption of genetically engineered
crops (58). More dramatic decreases are reported for the number of acre
treatments (number of acres times number of treatments per pesticide), a
measure that does not incorporate the volume of pesticide used.


In 1998 the area treated with chemicals traditionally used to combat the
European corn borer (ECB) was 7% less than in 1995, according to United
States Department of Agriculture (USDA) survey data compiled by the
National Center for Food and Agricultural Policy. Their unpublished, but
widely cited, report estimated that adoption of a new chemical accounted
for a 2% reduction, leaving a 5% reduction (4 million acres) unexplained
(60). The report attributed onehalf (2 million acres) of the unexplained
reduction in acreage treated with agrochemicals to the adoption of Bt corn
(18% of total acreage in 1998 versus 0% in 1995), a figure cited in
various media articles. The assumptions used to arrive at this figure are
not described, making the conclusion tenuous. Furthermore, as indicated in
the report, ECB infestation rates were up to 20 times lower in 1998 than
in 1995, raising the possibility that significant declines in acres
sprayed would have been observed even in the absence of Bt corn planting
(60). Comparisons of herbicide use on soybeans in 1995, when glyphosate
tolerant soybeans were not available, and in 1998, when they were,
revealed that on average more herbicides were applied in 1998 but in fewer
applications (61). The increase in herbicide usage is primarily due to a
7.3 times (SE 5 60.6, range 2.2 to 25.9) increase in pounds of glyphosate
used per acre and smaller increases in 7 other herbicides, accompanied by
declines in 16 other herbicides (62).

The trend between 1997 and 1998 suggests that adoption of genetically
engineered crops has resulted in an overall reduction of agrochemical use,
but some transgenic crops, such as glyphosate tolerant soybeans, have not.
Carefully designed experiments are needed to ascertain what effect
individual transgenic crops have on agrochemical use, independent of other
important variables, and the toxicity of the chemicals used needs to be
assessed. For example, are environmentally friendly chemicals replacing
more potentially harmful ones, or are we using a greater amount of
chemicals with comparable toxicity?

Soil conservation. Herbicide tolerant crops may lead to environmental
benefits by facilitating a shift to conservation tillage practices.
Specifically, these crops may allow farmers to eliminate pre-emergent
herbicides that are incorporated into the soil and rely on post-emergent
herbicides, such as glyphosate. The shift to postemergent control of weeds
may promote notill and conservation tillage practices that can decrease
soil erosion and water loss and increase soil organic matter (63). Studies
are needed to address whether soils are improving as a result of crops
genetically engineered for herbicide tolerance.

Increased yield. If genetically engineered crops increase yields, some
suggest that environmental benefits will include the preservation of
natural habitats because less land may be developed for agriculture.
Evidence indicates that transgenic crops in the United States have
increased yields somewhat, but like the data reported on pesticide use,
other factors may account for differences or the lack of differences
between transgenic and conventional crops (60, 64). However, the potential
environmental benefits of genetically engineered crops through increased
yield may be greatest in developing countries where agricultural output
may stand for the most improvement. Phytoremediation. Some genetic
modifications of plants or microorganisms may provide in situ remediation
of polluted soils, sediments, surface waters, and aquifers. Transgenic
plants can increase removal of toxic heavy metals from polluted soils and
waters and sequester these into plant tissue available for harvest
(65–67), or can transform pollutants into less toxic forms (68).
Environmental remediation through transgenic plants has not yet been used
widely, so net environmental benefits have not been measured.

Sustainability of GEOS: Implications for Risks and Benefits

For any crops with insecticidal properties, viral resistance, or herbicide
tolerance, the continued effectiveness or sustainability of these traits
is intricately connected to the evolution of resistance. Transgenic crops
that continuously express an insecticidal protein may lead to an increase
of insects resistant to the toxin. The diamondback moth (Plutella
xylostella) has developed resistance to Bt toxins sprayed in the field,
and at least 10 species of moths, 2 species of beetles, and 4 species of
flies have developed resistance under laboratory exposure to Bt toxins
(69). The evolution of resistance will, at the least, eliminate the
benefits associated with a particular genetically modified crop, and at
the most, resistance will have negative ecological consequences, if it
results in using harsher pesticides or more applications of pesticides.

Currently, insect resistance management advises a strategy that combines a
high dose exposure to toxin interspersed with planting refuges, areas
without the transgenic crop, to minimize the spread of resistance in a
population (70). Evidence indicates that a properly implemented refuge
strategy can slow the rate of resistance evolution (71–73) but does not
prevent it. Refuges of susceptible individuals are intentionally
maintained to mate with resistant individuals and produce offspring
vulnerable to high doses of insecticide. Gene flow between these two
groups depends on random mating between resistant and susceptible
individuals, dispersal before mating, and synchrony of breeding between
resistant and susceptible individuals. These conditions are sometimes met,
but not always (74–77).

The continued effectiveness of particular herbicide tolerant transgenic
crops is also uncertain. Herbicide tolerant weeds may evolve through the
transfer of herbicide tolerant traits by way of gene flow from transgenic
plants, or as a consequence of the increased use of a restricted number of
herbicides. Glyphosate, considered an environmentally friendly herbicide,
was used widely for 15 to 20 years without the evolution of weed
resistance to the herbicide; however, glyphosate tolerance is now known in
rigid ryegrass (Lolium rigidum), a pernicious grass weed. If glyphosate
resistance spreads, there is the concern that more toxic alternatives may
replace glyphosate.

Conclusions
1) Neither the risks nor the benefits of GEOs are certain or universal.
Both may vary spatially and temporally on a case by case basis.
Comparisons among transgenic, conventional, and other agricultural
practices, such as organic farming, will elucidate the relative risks and
benefits of adopting GEOs.

2) Our capacity to predict ecological impacts of introduced species,
including GEOs, is imprecise, and data used for assessing potential
ecological impacts have limitations. Our inability to accurately predict
ecological consequences, especially longterm, higher order interactions,
increases the uncertainty associated with a risk assessment and may
require modifications in our risk management strategies.

3) Additional or unidentified benefits and risks may exist that published
data do not yet address.

) Two aspects of genetic modification may warrant special consideration
for assessing risks. First, the quantity of modification and modified
products may differ from those available through traditional breeding
programs. As more economically useful and health related genes are
identified and isolated, it appears that the variety of GEOs will increase
dramatically. This increase may collectively represent an environmental
risk, given the limitations of predicting negative effects. Second, the
quality of modifications and modified products may also differ from those
available through selective breeding. Traditional breeding is limited by
the available genetic variability in the target organism or its relatives.
The great potential, as well as risk, of genetic engineering is that it
removes those limits, providing a greater range of possibilities for
transferring desired phenotypes into organisms.

5) Evaluation of potential environmental benefits, still in its infancy,
will allow risk managers and decision makers to balance these against the
extent and irreversibility of any ecological change. How we document the
benefits is critical. In particular, we should incorporate relative
environmental toxicity into analyses of changes in pesticide use and
quantify the impacts of herbicide tolerant crops on soil conservation. 6)
Measures that prevent transfer of genes that may negatively impact wild
populations and that slow the evolution of resistance to the transgenes
can minimize some of the possible ecological risks and can prolong the
possible benefits associated with genetically engineered plants.


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==========
1 AAAS Environmental Fellow, U.S. Environmental Pro
tection Agency, Office of Research and Development,
National Center for Environmental Assessment, 1200
Pennsylvania Avenue, N.W., (8601D), Washington, DC
20460, USA. 2 AAAS Diplomacy Fellow, U.S. Depart
ment of State, Bureau of Oceans, Environment, and
Science, 2201 C Street, N.W., Washington, DC 20520,
USA. The views presented here are solely those of the
authors and do not necessarily represent the views of
either agency or the United States government.

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Modified-Crop Studies Are Called Inconclusive

By CAROL KAESUK YOON
http://www.nytimes.com/2000/12/14/science/14BIOT.html
December 14, 2000

Ever since genetically modified crops appeared, supporters and detractors
of the plants have made competing claims about whether they are safe or
harmful to the environment.

Tomorrow, in what some scientists say is the first comprehensive review of
the published scientific data, researchers will report that simple
conclusions cannot yet be drawn because the crucial studies have not yet
been done.

Millions of acres of the crops have been planted in the United States,
their way paved by studies conducted by industry and submitted to
government regulators as evidence of safety but which typically were not
published in peer-reviewed journals.

For this review, the researchers examined only studies that other
scientists had determined were of high- enough quality to merit
publication.

The researchers found that while genetically engineered crops hold
potential for both risk and benefit, scientists still know little about
the likelihood even of the environmental threats of greatest concern.
Also, almost no studies have been published documenting ecological
benefits.

The two authors of the study published in the journal Science are fellows
sponsored by the American Association for the Advancement of Science, the
world's largest nonprofit scientific federation.

In their study, in which they call for new research, the authors say
current data indicate that assessing ecological risks is likely to be
complex, with risks varying among crops, even among strains of a single
crop, between environments and over time. Some risks, they say, may be so
difficult and time-consuming to assess as to be effectively unknowable.

"We're a ways away from really having answers," said Dr. LaReesa
Wolfenbarger, an ecologist who is doing her fellowship at the
Environmental Protection Agency and is co- author of the study with Dr.
Paul Phifer, a conservation biologist doing his fellowship at the State
Department. The authors emphasized that they had conducted the study
independently and did not speak for the government.

"Some of these questions are very elusive," Dr. Wolfenbarger said, "but
that doesn't mean that we stop studying them or make sweeping
generalizations that they don't exist."

Scientists on both sides of the debate called the review fair and
accurate, though each side interpreted the findings differently.

"It's a pretty reasonable summary and pretty well balanced," said Dr.
Robert Fraley, chief technical officer of the Monsanto Company.

Dr. Fraley played down the findings, however, saying that in several years
of commercial use, no ecological problems had yet been shown to be caused
by genetically engineered plants.

Dr. Jane Rissler, senior staff scientist at the Union of Concerned
Scientists, a group critical of the use of genetically modified crops,
called the paper "very fair and clear."

Dr. Rissler said: "You come out of this with a strong sense that we don't
know very much about the risks and the benefits. If we don't know, why are
we doing this?"

A spokeswoman for the Department of Agriculture, which oversees regulation
of genetically engineered plants, said scientists at the department were
reviewing the study.

The researchers examined 35 peer-reviewed studies. They looked at risks
including the production of "superweeds," the creation of new viral
diseases and unintended harm to nonpest species, like monarch butterflies.
They often found that while studies suggested a potential for risk, other
studies presented conflicting results arguing against risk. In some cases,
laboratory studies suggested risk, but no studies in the field were
conducted to test if harm occurred.

And while some studies showed the potential for environmental benefits
from these crops, the researchers found they fell short of documenting
actual benefit.

For example, a Department of Agriculture study indicated a 1 percent
decrease in the amount of pesticides used on corn, cotton and soybeans in
1998, as an apparent result of the adoption of genetically modified crops.
Yet, Dr. Wolfenbarger said, it remains unknown whether this decrease in
pesticides translated into any environmental benefit for wild species.