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THE MONARCH BUTTERFLY CONTROVERSY |
The second most widely
grown transgenic crop in the United States are maize (Zea
mays) cultivars that have been engineered to express genes for
various insecticidal protein endotoxins (Bt toxins) from
the soil bacterium Bacillus thuringiensis. The principal target species for Bt toxin-expressing maize
(Bt maize) is the European corn borer (Ostrinia
nubilalis), one of the most damaging pests of maize in North
America. Losses attributable to European corn borer damage exceed over
$1 billion annually in the United States alone. Bt
toxins are widely believed to be selectively toxic, only affecting
those insects (e.g. lepidopteran larvae) that have a gut alkaline
enough to activate the Bt protoxin by enzymatic
proteolysis. Receptor binding by the C-terminal domain of the active
toxin is the major determinant of host specificity by the different
Bt toxins.
Given the growing agricultural importance of Bt maize as
well as Bt cotton (Gossypium hirsutum)
and Bt potato (Solanum tuberosum), it is not surprising that a storm of controversy arose following the
publication in Nature of a preliminary study by Losey et
al. (1999)
. This paper raised serious concerns about the ecological safety of Bt maize cultivation to non-target
lepidopterans, in particular the larvae of monarch butterfly
(Danaus plexipus). On the basis of laboratory assays,
the authors concluded that monarch larvae reared on milkweed
(Asclepias syriaca) leaves dusted with pollen from
Bt maize ate less, grew more slowly, and suffered higher
mortality than those reared on leaves dusted with nontransformed maize
or on leaves without pollen.
The conclusions of Losey et al. (1999) were challenged on three
grounds. First, the pollen doses used by Losey et al. (1999) were not
quantitatively measured but were gauged by eye to match pollen dustings
on milkweed leaves collected in the field. This raised concerns about
subconscious biases on the part of the researchers. Second, concerns,
as it turns out, valid ones, were raised as to the validity of
extrapolating from the results of Losey at al. (1999), which concerned
only one type of pollen, to all types of Bt maize
pollen. Third, the soundness of extrapolating from laboratory assays to
the field was uncertain, although a subsequent field study by Jesse and
Obrycki (2000) did seem to confirm the fears raised by the Losey et al.
(1999) study.
Regardless of the deficiencies of the study, the results of Losey et
al. (1999) were widely heralded by the popular press and established
the monarch butterfly, one of the more beautiful creatures on our
planet, as the cause célèbre for environmentalists opposed
to biotechnology. Berenbaum (2001) has written an engaging piece
concerning the diametric responses that the lay and scientific presses
have had as this controversy has unfolded.
This month's "The Hot and the Classic" is devoted to summarizing
some new contributions that specifically address the question of the
risk associated with Bt maize pollen to the monarch butterfly.
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Field Studies |
To interpret accurately the results of studies that examine the
effects of Bt maize pollen on monarch larvae, it is
necessary to know the range and distribution of naturally occurring
pollen densities on milkweed leaves. This gap in our knowledge has
recently been filled by Pleasants et al. (2001), who measured the
density of maize pollen on milkweed plants inside and outside of maize fields in several different localities. Average pollen density was
highest within maize fields (171 grains per cm2) and was
progressively lower from the field edge outward, falling to 14 grains
per cm2) at 2 m (see also Jesse and Obrycki, 2000;
Wraight et al., 2000). The authors also describe complexity in the
pattern of maize pollen density within the canopies of milkweed plants.
Younger milkweed leaves, which typically harbor more than half of the
monarch larvae, have on average only 30% to 50% of the pollen density
of middle leaves due to their greater exposure to cleansing rain and to their steeper leaf angles. Rain is a principal determinant of pollen
density: A single rainfall can remove 54% to 86% of the maize pollen
on milkweed leaves.
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Not All Transgenic Pollen Is Toxic |
Transgenic maize hybrids that are currently or have been
commercially available contain cry1Ab (events Bt11,
Mon810, and 176), cry9c (event Cbh351), or
cry1Ac (event Dbt418) Bt genes. In
addition, registration was recently granted for a hybrid that expresses a cry1F gene (event Tc1507). Because the initial report
by Losey et al. (1999) examined the effects of only one type of
transgenic pollen (Cry1Ab event 176), Hellmich et al. (2001) conducted
laboratory tests to establish the relative toxicity of various other
Bt toxins to monarch larvae (see also Wraight et al.,
2000). Bioassays of purified Bt toxins indicate that
Cry9C and Cry1F proteins are relatively nontoxic to monarch first
instars, whereas first instars are sensitive to Cry1Ab and Cry1Ac
proteins. Older instars were 12 to 23 times less susceptible to Cry1Ab
than were first instars. Pollen bioassays indicated that pollen
contaminants, mostly fractured anthers, were particularly toxic to
larvae. This finding suggests that caution must be exercised in
interpreting the findings of Jesse and Obrycki (2000), who used pollen
preparations containing 6 times more contaminants than the preparations
of Hellmich et al. (2001). The only transgenic maize pollen that
consistently affected monarch larvae was from Cry1Ab event 176 hybrids,
currently less than 2% of the maize planted and for which
reregistration has not been applied. The authors conclude that pollen
from the Cry1Ab (events Bt11 and Mon810) Cry1F, and Cry9C hybrids will have no acute effects on monarch larvae in the field.
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Risk Assessment Studies |
A proper risk assessment of the impact of Bt
maize cultivation on monarch butterfly populations requires
consideration of both the expression of toxicity and the likelihood of
exposure to the toxin. A collaborative research effort by scientists in Canada and the United States gathered information concerning the acute
toxic effects of Bt maize pollen and the degree to which monarch larvae would be exposed to toxic amounts (Sears et al., 2001).
The authors estimate that even if harmful Bt maize (event 176) cultivation were to climb to 80% of the total cultivated maize,
only 6% of the monarch larval population would be at risk. If
nonharmful cultivars (Mon 810 and Bt11) were to climb to 80% of total
maize cultivation, the percentage of monarchs at risk would fall to
0.05%. The authors conclude that the impact of Bt maize
pollen from current commercial hybrids on monarch butterfly populations
is negligible.
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Bt Maize versus Conventional Pesticides |
Losey et al. (1999) concluded their report with the
recommendation that "... we gather the data necessary to evaluate
the risks associated with the new agrotechnology and... compare
these risks with those posed by pesticides and other pest-control
tactics." Toward this goal, Stanley-Horn et al. (2001) undertook to
compare the effects on monarch larvae of pollen from cultivars of
Bt-expressing maize, both harmful and harmless, with
those of nontransgenic maize sprayed with a conventional chemical
pesticide (
-cyhalothrin). As expected, they found that event 176 Bt pollen, even at low densities (23-67 pollen grains
cm
1), had deleterious effects on monarch larvae, whereas
the pollen of other Bt maize cultivars (Bt11 or Mon810)
was essentially harmless. The reduction in survivorship and weight gain
seen with the harmful event 176 pollen was dwarfed by the effects of
the pesticide -cyhalothrin, which is commonly used as a chemical
treatment against European corn borers. Most larvae died within hours
after feeding on milkweed leaves collected from plants exposed to spray
application. Survival and growth of larvae feeding on milkweed outside
of the sprayed plots was also reduced because of insecticidal drift.
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Effects on Other Nontarget Lepidoptera |
Zangerl et al. (2001) concluded that Bt maize
incorporating event 176 does have sublethal effects on black
swallowtails (Papilio polyxenes) in the field. An
earlier study by Wraight et al. (2000), however, failed to detect an
effect of harmless Bt pollen (Mon810) on black swallowtails.
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Conclusion |
Losey et al. (1999) should be lauded for uncovering and exposing
the nontarget effects of event-176 maize pollen on monarch larvae.
Their publication had the salutary effect of raising both the
consciousness of the public and of the biotechnology industry of the
possible nontarget effects of Bt crops. However, those individuals and organizations who attempted to extrapolate the results
of Losey et al. (1999) to other strains of Bt maize, and to Bt crops in general, have now been shown to be in
error at least in regard to the monarch butterfly. The effects of
Bt maize cultivation on monarch butterfly maize
populations are negligible, and current evidence suggests that
Bt maize is an environmentally safer insect control
strategy than conventional chemical spraying.
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THE MONARCH BUTTERFLY...
Field Studies