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of GM crops outside the United States, where the precautions necessary to prevent gene
flow and insect resistance may not be practical. Gene flow may be of particular concern
in tropical areas where the wild relatives of many agricultural crops are endemic and the
hectarage dedicated to the cultivation of GM crops is increasing.
In general, the results of risk assessments of GM crops indicate, to date, that there are
few to no consistent negative effects of
Bt
protein, the cultivation of
Bt
plants, or
Bt
plant
residues on most of the soil bacteria, saprotrophic and pathogenic fungi, protozoa, earth-
worms, and microarthropods evaluated. When significant effects have been detected, they
have often been minimal or transitory, making their ecological significance difficult to
assess. While the research conducted thus far is by no means exhaustive, it is encouraging
to note that few negative effects have been detected on soil organisms, despite the wide-
spread and long-term cultivation of
Bt
crops. The soil organisms that appear to be most
sensitive to
Bt
crop cultivation include AMF, nematodes, and nontarget insect larvae that
live or feed in soil in close proximity to areas
cultivated with
Bt
crops.
As nontarget effects cannot always be attributed to a particular Cry protein, risk
assessment research should include investigations to identify genetic alterations that pro-
duce a change in the physiology or tissue composition of the plant. A genetic insertion that
results in a change in plant root exudates, for example, could influence species composi-
tion in the rhizosphere without being an effect of the
Bt
protein itself. Internationally, more
research funding should be directed toward risk assessment of GM plants in the areas of
fungal ecology, nematode abundance and diversity, and insect ecology in both terrestrial
and aquatic ecosystems. Moreover, each new GM plant line should be tested for effects on
nontarget organisms under a variety of environmental and experimental conditions, as
results of previous studies varied depending on biotic and abiotic factors that may or may
not be associated with the expression
of
Bt
proteins. Researchers should also continue to
investigate nontarget effects on symbionts that improve plant performance (e.g., nitrogen-
fixing bacteria, AMF), as these are soil organisms that may be most sensitive to
Bt
proteins
or to cultivation of
Bt
crops because of their dependence on a plant host. A focus on long-
term field experiments and collaborative research efforts between soil ecologists, agro-
ecologists, microbial ecologists, and others will help to understand better the long-term
effects of the cultivation of
Bt
crops on multitrophic-level interactions (e.g., Hilbeck et al.,
1999; Groot and Dicke, 2002; Guo et al., 2008) and ecosystem functioning. Future investiga-
tions should incorporate the use of molecular tools for the identification and quantification
of different trophic groups of soil microorganisms, as plate counts and other culturing
methods are generally not sufficiently specific. As more and different types of
Bt
crops
are developed, it will be important to evaluate the effects of each genetic insertion event
on a variety of nontarget organisms under different environmental and experimental sce-
narios. Allocating sufficient resources to postrelease monitoring will also be important
for mitigating any potential negative effects of the cultivation of GM crops on nontarget
organisms in both terrestrial and aquatic ecosystems.
The preparation of this review and the
Bt
maize-AMF research herein by T. E. Cheeke
was supported by the Charles A. and Anne Morrow Lindbergh Foundation, the U.S.
Environmental Protection Agency (EPA) under the Science to Achieve Results (STAR)
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