Although plants transformed with genetic material from
the bacterium Bacillus thuringiensis (Bt) are generally
thought to have negligible impact on non-target organisms1,
Bt corn plants might represent a risk because most hybrids
express the Bt toxin in pollen2, and corn pollen is dispersed
over at least 60 metres by wind3. Corn pollen is deposited
on other plants near corn fields and can be ingested by
the non-target organisms that consume these plants. In a
laboratory assay we found that larvae of the monarch butterfly,
Danaus plexippus, reared on milkweed leaves dusted with
pollen from Bt corn, ate less, grew more slowly and suffered
higher mortality than larvae reared on leaves dusted with
untransformed corn pollen or on leaves without pollen.
Pollen for our assay was collected from N4640-Bt corn and
an unrelated, untransformed hybrid, and was applied by gently
tapping a spatula of pollen over milkweed (Asclepias curassavica)
leaves that had been lightly misted with water. Pollen density
was set to visually match densities on milkweed leaves collected
from corn fields. Petioles of individual leaves were placed
in water-filled tubes that were taped into plastic boxes.
Five three-day-old monarch larvae from our captive colony
were placed on each leaf, and each treatment was replicated
five times. Milkweed leaf consumption, monarch larval survival
and final larval weight were recorded over four days.
Larval survival (56%) after four days of feeding on leaves
dusted with Bt pollen was significantly lower than survival
either on leaves dusted with untransformed pollen or on
control leaves with no pollen (both 100%, P=0.008) (Fig.
1a). Because there was no mortality on leaves dusted with
untransformed pollen, all of the mortality on leaves dusted
with Bt pollen seems to be due to the effects of the Bt
toxin.
<Picture>Figure 1 Survival and leaf consumption
of second- to third-instar monarch larvae on each of three
milkweed leaf treatments: leaves with no pollen (light blue),
leaves treated with untransformed corn pollen (green) and
leaves dusted with pollen from Bt corn (dark blue). Full
legend
There was a significant effect of corn pollen on monarch
feeding behaviour (P=0.0001) (Fig. 1b). The mean cumulative
proportion of leaves consumed per larva was significantly
lower on leaves dusted with Bt pollen (0.57 <Picture>
0.14, P=0.001) and on leaves dusted with untransformed pollen
(1.12 <Picture> 0.09, P=0.007) compared with consumption
on control leaves without pollen (1.61 <Picture> 0.09).
The reduced rates of larval feeding on pollen-dusted leaves
might represent a gustatory response of this highly specific
herbivore to the presence of a 'non-host' stimulus. However,
such a putative feeding deterrence alone could not explain
the nearly twofold decrease in consumption rate on leaves
with Bt pollen compared with leaves with untransformed pollen
(P=0.004).
The low consumption rates of larvae fed on leaves with
Bt pollen led to slower growth rates: the average weight
of larvae that survived to the end of the experiment on
Bt-pollen leaves (0.16 <Picture> 0.03 g) was less
than half the average final weight of larvae that fed on
leaves with no pollen (0.38 <Picture> 0.02 g, P=0.0001).
These results have potentially profound implications for
the conservation of monarch butterflies. Monarch larvae
feed exclusively on milkweed leaves4; the common milkweed,
A. syriaca, is the primary host plant of monarch butterflies
in the northern United States and southern Canada5. Milkweed
frequently occurs in and around the edges of corn fields,
where it is fed on by monarch larvae6. Corn fields shed
pollen for 8-10 days between late June and mid-August, which
is during the time when monarch larvae are feeding7. Although
the northern range of monarchs is vast, 50% of the summer
monarch population is concentrated within the midwestern
United States, a region referred to as the 'corn belt' because
of the intensity of field corn production8. The large land
area covered by corn in this region suggests that a substantial
portion of available milkweeds may be within range of corn
pollen deposition.
With the amount of Bt corn planted in the United States
projected to increase markedly over the next few years9,
it is imperative that we gather the data necessary to evaluate
the risks associated with this new agrotechnology and to
compare these risks with those posed by pesticides and other
pest-control tactics.
John E. Losey, Linda S. Rayor, Maureen E. Carter,
Department of Entomology, Comstock Hall, Cornell University,
Ithaca, New York 14853, USA, e-mail: jel27@cornell.edu
References
1.Ostlie,
K. R., Hutchison, W. D. & Hellmich, R. L. Bt Corn and
European Corn Borer (NCR publ. 602, Univ. of Minnesota,
St Paul, 1997).
2.Fearing,
P. L., Brown, D., Vlachos, D., Meghji, M. & Privalle,
L. Mol. Breed. 3, 169-176 (1997).
3.Raynor,
G. S., Ogden, E. C. & Hayes, J. V. Agron. J. 64, 420-427
(1972).
4.Malcolm,
S. B., Cockrell, B. J. & Brower, L. P. in Biology and
Conservation of the Monarch Butterfly (eds Malcolm, S. B.
& Zalucki, M. P.) 253-267 (Natural History Museum of
Los Angeles County, Los Angeles, 1993).
5.Malcolm,
S. B., Cockrell, B. J. & Brower, L. P. J. Chem. Ecol.
15, 819-853 (1989).
6.Yenish,
J. P., Fry, T. A., Durgan, B. R. & Wyse, D. L. Weed
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7.Brower,
L. P. J. Exp. Biol. 199, 93-103 (1996).
8.Wassenaar,
L. I. & Hobson, K. A. Proc. Natl Acad. Sci. USA 95,
15436-15439 (1998).
9.Andow,
D. A. & Hutchison, W. D. in Now or Never: Serious New
Plans to Save a Natural Pest Control (eds Mellon, M. &
Rissler, J.) 19-65 (Union of Concerned Scientists, Cambridge,
Massachusetts, 1998).
Macmillan
Magazines, Nature (c) Macmillan Publishers Ltd 1999 Registered
No. 785998 England.
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