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Assessing the impact of Cry1Ab-expressing corn
pollen on monarch butterfly larvae in
field studies
Diane E. Stanley-Horn*†, Galen P. Dively‡, Richard L. Hellmich§, Heather R. Mattila*, Mark K. Sears*, Robyn Rose‡,
Laura C. H. Jesse¶, John E. Losey
ʈ, John J. Obrycki¶, and Les Lewis§
*Department of Environmental Biology, University of Guelph, Guelph, ON, Canada N1G 2W1; ‡Department of Entomology, University of Maryland, College Park, MD 20742; §United States Department of Agriculture, Agricultural Research Station, Corn Insects and Plant Genetics Research Unit, ¶Department of Entomology, Iowa State University, Ames, IA 50011-3140; and ʈDepartment of Entomology, Cornell University, Ithaca, NY 14853 Edited by M. R. Berenbaum, University of Illinois at Urbana-Champaign, Urbana, IL, and approved August 22, 2001 (received for review June 4, 2001) Survival and growth of monarch larvae, Danaus plexippus (L.),
mine the impact of Bt pollen on the survival and growth of D. after exposure to either Cry1Ab-expressing pollen from three
plexippus. Each study varied in experimental design and treat- Bacillus thuringiensis (Bt) corn (Zea mays L.) events differing in
ments tested; however, the general approach was to expose toxin expression or to the insecticide, -cyhalothrin, were exam-
larvae to milkweed leaves containing natural deposits of Bt and ined in field studies. First instars exposed to low doses (Ϸ22 grains
non-Bt pollen that accounted for pollen accumulation, natural per cm2) of event-176 pollen gained 18% less weight than those
degradation of toxin within pollen of various ages under differ- exposed to Bt11 or Mon810 pollen after a 5-day exposure period.
ent environmental conditions, and the possible ingestion of Larvae exposed to 67 pollen grains per cm2 on milkweed leaves
Bt-expressing plant material other than pollen. In the Maryland from within an event-176 field exhibited 60% lower survivorship
study, the responses of larvae to pollen were compared with and 42% less weight gain compared with those exposed to leaves
responses to an insecticide used to control Ostrinia nubilalis.
from outside the field. In contrast, Bt11 pollen had no effect on
growth to adulthood or survival of first or third instars exposed for

5 days to Ϸ55 and 97 pollen grains per cm2, respectively. Similarly,
Iowa Study I. A split-split plot experiment was conducted on two no differences in larval survivorship were observed after a 4-day
Iowa State University farms planted on May 24, 2000 with six Bt exposure period to leaves with 504 –586 (within fields) or 18 –22
hybrids: NK3030Bt, NK7070Bt (Syngenta Seeds, Golden Valley, (outside the field) pollen grains per cm2 collected from Bt11 and
MN; Bt11 event), 38G17, 34R07 (Pioneer Hi-Bred, Des Moines, non-Bt sweet-corn fields. However, survivorship and weight gain
IA; Mon810 event), Maximizer 21 (Syngenta Seeds; event 176), were drastically reduced in non-Bt fields treated with -cyhalo-
and 2249 (Mycogen Seeds, Indianapolis, IN; event 176). The thrin. The effects of Bt11 and Mon810 pollen on the survivorship
non-Bt hybrids NK3030, NK7070 (Syngenta), 3489, and 3893 of larvae feeding 14 to 22 days on milkweeds in fields were
(Pioneer Hi-Bred) were included as controls. The transforma- negligible. Further studies should examine the lifetime and repro-
tion events were randomly assigned as main-plot treatments to ductive impact of Bt11 and Mon810 pollen on monarchs after
four complete blocks on each farm. Plots measured 4.6 by 4.6 m long-term exposure to naturally deposited pollen.
and were separated by Ն18.3 m of soybeans to minimize pollen drift among plots (9). Subplots were potted A. syriaca plants Corn(ZeamaysL.)hasbeentransformedwithagenefromthe placed at two locations per plot Ϸ2 days before corn anthesis,
bacterium Bacillus thuringiensis (Bt) to express the insecti- with two in the middle and two at the edge of the plot. When cidal 1 epidopteran-active crystalline protein (Cry1Ab) endo- 50–75% of the corn plants had shed pollen, three first-instar toxin (1). The Cry1Ab toxin is specifically active on the lepidop- monarch larvae (Ͻ24-h old) were transferred to leaves on the teran species so the impact on nontarget organisms has been upper half of each milkweed plant. One plant from each subplot considered negligible (2). However, most commercial Bt corn was caged with fine-mesh screening to deter predation. Before hybrids express the toxin in the pollen (3) that may be deposited larval infestation, a leaf was selected randomly from the upper on host plants of nontarget species. In particular, the monarch half of each plant and brought back to the laboratory where butterfly, Danaus plexippus (L.) may be at risk (4, 5), because pollen grains were counted in five randomly chosen 0.25-cm2 monarch larvae feed on the common milkweed, Asclepias syriaca sections of the leaf by using an ocular grid and a stereo (6), in and near cornfields. About half of the overwintering microscope. Five days after infestation, larval survival and monarch population originates from the region known as the weight were recorded. Each leaf then was removed from the Corn Belt (7), so a portion of the migratory monarch population upper half of each plant for a second determination of pollen may be exposed to Bt pollen. However, the exposure of monarch larvae to the Cry1Ab toxin varies for different Bt corn events.
Pollen from event-176 Bt hybrids expresses the highest level of Ontario Study. The study was conducted in six commercial field- corn sites [4.9–17.4 hectares (ha)] planted within Wellington ␮g͞g of pollen; http:͞͞www.epa.gov͞ pesticides͞biopesticides͞factsheets͞fs006458t.htm) and has County, Ontario, Canada in May 2000. Three Bt11 fields (two been demonstrated to have adverse effects on first-instar mon- N2555 and one N27 M3, Syngenta Seeds) and three non-Bt fields arch caterpillars (5, 8). The registration of hybrids derived from (Pride 177, Pioneer Hi-Bred; Hyland 2240, Hyland Seeds, Blen- event 176 will terminate in 2001 (http:͞͞www.epa.gov͞scipoly͞ sap͞2000͞october͞brad1 execsum overview.pdf). Bt11 and This paper was submitted directly (Track II) to the PNAS office.
(http:͞͞www.epa.gov͞scipoly͞sap͞2000͞october͞), so the po- Abbreviations: Bt (Bacillus thuringiensis); Cry1Ab, 1 epidopteran-active crystalline protein;ha, hectares.
tential negative impacts of these hybrids may be lower than that †To whom reprint requests should be addressed. E-mail: destanle@uoguelph.ca.
Reported herein are five independent field studies conducted The publication costs of this article were defrayed in part by page charge payment. Thisarticle must therefore be hereby marked “advertisement” in accordance with 18 U.S.C.
in Iowa, Maryland, Ontario (Canada), and New York to deter- §1734 solely to indicate this fact.
www.pnas.org͞cgi͞doi͞10.1073͞pnas.211277798 PNAS ͉ October 9, 2001 ͉ vol. 98 ͉ no. 21 ͉ 11931–11936
heim, ON, Canada; and 4064NK, Syngenta Seeds) were selected between hybrid treatments, and each block was surrounded by a based on whether they were Ͼ150 m from other cornfields and 9-m buffer zone of bare ground to minimize drift effects. Plants had naturally occurring milkweed in the following locations: Ϸ1 were propagated and transplanted as described above. Two m inside the field, Ͻ1 m from the field edge, and Ϸ5 m from the plants were transplanted at 3 m from the inside edge (between field edge, along eight transects perpendicular to the field edge.
rows 4 and 5) and the outside edge of each hybrid plot, along As controls, eight naturally occurring milkweed plants were transects evenly spaced along the field edge. The air-blast selected in each of three natural areas situated Ͼ150 m from any sprayer ran between the edge of the plot and the outside milkweeds, so these plants were not exposed to the directed The eight transects were alternately assigned to one of two spray. Separate bioassays were conducted at 3, 6, and 9 days after bioassays that began on day 6 and day 11 of anthesis, respectively.
the onset of anthesis, as described above. Leaves were removed For each bioassay, a cohort of five larvae, reared on A. syriaca within 1 h after insecticide treatments that coincided with the in the laboratory, was weighed, randomly assigned to a plant, and placed on the upper third of the plant. The whole plant was then enclosed in a fine mesh cage to deter predation. Larvae for the Iowa Study II. A replicate field site subdivided into paired 0.2-ha first bioassay were first instars (12- to 36-h old), whereas those plots of N4640Bt corn (Syngenta Seeds; Bt11 event) and non-Bt used in the second bioassay were third instars (Ͻ24 h post second N4640 corn (Syngenta Seeds) was planted in late April 2000 at molt). After a 5-day exposure period, the number and instar of each of three Iowa State University farms. Milkweed plants were larvae were recorded. Larval cohorts were brought back to the transplanted to the field sites during May and June. Six plants laboratory where they were weighed and reared to adulthood on (5–50 cm tall) were established at each of three locations: 4.6 m clean A. syriaca at 24°C and a 16-h light͞8-h dark cycle. Addi- inside the plot, at the field edge, and 2 m from the plot edge. Five tional data were recorded on days to pupation, pupal weight, first instars were placed on each plant Ϸ7 days after the start of percentage of pupation and emergence, and adult weight and anthesis. The number and life stages of larvae were recorded wing length. Leaves with feeding damage were collected from every 24 h for the first 7 days, and then every 48 h for another plants of the first bioassay and viewed with a video imaging 7 days. Leaves were collected and pollen densities were esti- system (XC-75CE, Cosmicar͞Pentax 16-mm camera with mated at 3–8 days after larval introduction by counting the NORTHERN EXPOSURE V.2.9E software, Empix Imaging, Missis- number of grains on one 0.5-cm2 leaf disk excised with a #6 cork sauga, ON, Canada) to estimate the area of consumption. Pollen borer from a middle leaf of each plant (5).
densities were determined for leaves collected from the tops, middles, and bottoms of plants. To minimize the loss of pollen, New York Study. One 0.25-ha field near Ithaca, NY was planted all sampled leaves were sandwiched between strips of contact in two 36-row sections, one with the Bt hybrid 36-G32Bt (Pioneer paper (ConTact7 Brand; Decora Manufacturing, North Rid- HiBred, Mon810 event) and the other with a non-Bt corn hybrid geville, OH). Pollen counts within five 1-cm2 areas on the tops (3752). Ten milkweed plants were transplanted at three locations and bottoms of leaves were added to corresponding counts in the in each section: along the edge, and at 6.6 and 32.7 m inside the contact paper to obtain density estimates. Grains adhering to the field. At Ϸ2 days from the onset of pollen shed, five first instars paper were stained with acid fuchsin (Sigma) to facilitate were placed on each plant. The number and life stages of larvae were recorded every 24 h for 22 days. The pollen density on each plant was measured 6 days after larval introduction according to Maryland Study. Field-corn experiment. The study was conducted the same methods used in the Iowa II study.
in an 8-ha cornfield at the University of Maryland Research and Education Center at Beltsville, MD. The field was planted on Data Analysis. In the Maryland study, variances of data not May 3, 2000 with the hybrid TM5114 (Mycogen Seeds; event meeting the assumptions of ANOVA were grouped before 176). Milkweed plants were propagated from rhizomes in 20-cm analysis (10). In the Ontario and Iowa I studies, log or arcsine pots and grown outdoors until they were 50–60 cm in height.
transformations were applied as required. In all three experi- Two transects of milkweeds treated as blocks were established ments, the following variables for each bioassay were analyzed by along each side of the field before anthesis. At each transect, ANOVA (PROC MIXED; ref. 11): pollen deposition, percentage of plants were transplanted within and outside the field at Ϫ10, Ϫ5, survival and weight gain, and in the Ontario study, development, Ϫ3, Ϫ1 m, and 1, 3, 5, and 10 m from the field edge, respectively.
consumption, days to pupation, pupal and adult weights, percent Separate bioassays with field-collected leaves from each plant emergence, and adult wing length. In all studies, corn hybrid position were conducted at 3, 6, 9, and 14 days after the onset of treatment and milkweed position were treated as fixed effects, anthesis. At each time, pollen densities were estimated by whereas block or field was treated as a random effect. For the counting the number of grains in a 0.34-cm2 viewing area on a Iowa I data, bioassay type (caged or uncaged) was treated as a single leaf that was removed from the upper one-third of each fixed subplot factor. In addition, orthogonal contrasts were milkweed plant. Each leaf then was infested with a cohort of 10 conducted to test for differences between each Bt11 and Mon810 first instars (Ϸ24-h old) for 4 days. Survival and weights of larval hybrid and their isolines, and between the event-176 hybrids vs.
cohorts were assessed both initially and after 4 days.
the other two Bt hybrids combined. Means were separated with Sweet-corn experiment. The study was conducted at the Uni- Tukey’s studentized range test (P Ͻ 0.05). For the Iowa II and versity of Maryland Research and Education Center at Upper New York studies, the number of larvae alive over time was Marlboro, MD. The plot was planted on May 12, 2000 and analyzed by ANOVA (PROC GLM). Survival curves for larvae consisted of three hybrid treatments: untreated Attribute were analyzed separately for each hybrid with LIFETEST (SAS GSS0937 (Bt), untreated Prime Plus (non-Bt isoline), and treated Prime Plus, replicated four times in a randomized block design.
The Attribute hybrid (Syngenta Seeds) was developed by cross- ing with the Cry1Ab (Bt11 event) field corn and then backcross- Iowa Study I. Average pollen densities ranged from 21 to 23 grains ing to produce a pure inbred of Bt sweet corn. The treated non-Bt per cm2 across hybrid treatments, which were not significantly plots received three applications of ␭-cyhalothrin (Warrior 1E, different. These levels were relatively low compared with pub- Syngenta Crop Protection) delivered at the 94.6-ml formulation lished reports of pollen deposition (12) that could be a small-plot rate by an air-blast sprayer in 536 liters of spray volume per ha.
effect. Only the plant location effect was significant (P ϭ 0.027), Each of the four replicate blocks were planted with 4-m buffers showing higher pollen levels in the middle of the plot (26 grains 11932 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.211277798
Table 1. Comparison of survivorship and growth for Monarch larvae exposed as first or third instars to Bt11 and non-Bt pollen on
caged milkweed (A. syriaca
) plants in Ontario
*Day 5 avg instar͞day 0 avg instar.
†Day 6 avg wt͞day 0 avg wt.
‡Days to pupation from the beginning of the exposure period.
per cm2) compared with the plot edge (18 grains per cm2). For anthesis were 8.2, 63.7, 161.2, and 27.8 grains per cm2, respec- caged tests, average weights ranged from 2.8 to 3.3 mg per larva, tively. Average levels outside the field peaked at 18.5 grains per and all main and interaction effects were nonsignificant. For the cm2 on day 9 and significantly dropped off along positions uncaged tests, no significant effects also were indicated by using extending away from the field edge. The relative differences in the general linear model; however, the contrast test showed that pollen deposition across transect positions on each date were the average weights of larvae (1.7 mg) that fed on leaves with not the same (P ϭ 0.0015). During anthesis, seven rain events event-176 pollen were significantly less than weights of larvae (11–25 mm per day) occurred that may have washed pollen off (2.0 mg) on the other Bt hybrids combined (P ϭ 0.037). For percent survival, the hybrid treatment and all interaction effects Survival of monarch larvae ranged from 57.5 to 86.3% on day with hybrid were not statistically significant. However, both the 3 of anthesis (Fig. 1). Survivors, which initially weighed an plant location (P ϭ 0.002) and bioassay-type (caged or uncaged; P Ͻ 0.001) effects were significant. Survival was significantly higher at the plot edge (53.6%) and in caged cohorts (61.2%), compared with the middle of the plot (38.1%) and uncaged cohorts (30.5%), respectively. Predatory insects may have used the plots as a refuge to escape the prevailing hot-dry conditions in Iowa, resulting in higher predation in the middle of the field compared with the soy buffers surrounding the field. Also, lower predation seemed to occur in caged cohorts.
Ontario Study. Pollen densities on leaves did not differ between hybrid types (Bt or non-Bt) but decreased significantly with increasing distance from the field on day 6 (P Ͻ 0.0001) and day 11 (P Ͻ 0.0001) of anthesis. On day 6, the ranges of pollen densities at each distance were 2–309, 0–176, and 0–75 grains per cm2 for plants found at Ϫ1 m within the field, Ͻ1 m outside the field, and 5 m outside the field, respectively. On day 11, the range of densities calculated on leaf samples taken from Ϫ1, Ͻ1, and 5 m were 3–429, Ͻ1–320, and Ͻ1–50, respectively. Control plants contained Ϸ1 grain per cm2 on both days, probably resulting from contamination during leaf sampling. Average accumulated rainfall during the first 6 and 11 days of pollen shed (before placing cages on plants) was Ϸ10 and 13 mm, respectively, and may have washed pollen off of the plants (12).
The comparison of responses to Bt and non-Bt pollen is presented in Table 1. Neither hybrid type nor plant position affected survivorship, developmental rate, or weight gain of first- or third-instar monarchs during the exposure period in the field or in later developmental stages (but see % emergence for first instars in Table 1). No significant differences in survivorship, weight gain, or development to adulthood were observed be- tween larvae in cages within the fields and those in control cagesϾ150 m from any cornfield in either bioassay (P Ն 0.15 for all Survival of first-instar monarch larvae feeding on milkweeds placed at 1, 3, 5, and 10 m inside (negative values) and outside the field edge ofevent-176 field corn in Maryland. Means Ϯ SE are based on separate bioassays Maryland Study. Field-corn experiment. The average pollen den- conducted on days 3, 6, 9, and 14 of anthesis. Within each graph, columns with sities on milkweed leaves in the field on days 3, 6, 9, and 14 of the same letters are not significantly different (P Ͻ 0.05; Tukey’s test).
PNAS ͉ October 9, 2001 ͉ vol. 98 ͉ no. 21 ͉ 11933
Survival and weight gain of first-instar monarch larvae feeding on Weight gain of first-instar monarch larvae feeding on milkweeds milkweeds placed at 3 m inside and outside the edge of plots consisting of placed at 1, 3, 5, and 10 m inside (negative value) and outside the field edge Bt11, non-Bt (untreated), and non-Bt (␭-cyhalothrin-treated) sweet corn in of event-176 field corn in Maryland. Means Ϯ SE are based on separate Maryland. Data are based on separate bioassays conducted at 3, 6, and 9 days bioassays conducted on days 3, 6, 9, and 14 of anthesis. Within each graph, of anthesis. Within each graph, columns with the same lowercase letters are columns with the same letters are not significantly different (P Ͻ 0.05; Tukey’s not significantly different for the interaction effect; pairs of columns with the same uppercase letters are not significantly different for the treatment effect(P Ͻ 0.05; Tukey’s test).
average of 0.9 mg, gained 9.9 to 12.8 mg after 4 days (Fig. 2). On day 6, the plant position had a significant effect on larval survival rately for each bioassay date and are summarized in Fig. 3. On (P Ͻ 0.0001) and weight gain (P ϭ 0.0081). Sixty-three percent all dates, the treatment by position-interaction effect on per- of the larvae survived and gained 8.3 mg each after feeding on centage of survival was significant (day 3, P Ͻ 0.0001; day 6, P Ͻ leaves outside the field, compared with 25.1% survival and 0.0001; day 9, P ϭ 0.0027). Survival of monarch larvae feeding weight gains of 4.8 mg inside. On day 9, larval survival inside the on milkweed leaves either inside or outside Bt and non-Bt field was reduced by 51% compared with survival of milkweeds (unsprayed) plots ranged from 79.9 to 93.2% and were not located outside (P ϭ 0.0215). Larvae also gained less weight statistically different at any date. Survival of larvae feeding on inside the field, but differences across plant positions were not leaves collected inside and outside non-Bt (sprayed) plots was significant. On day 14, weight gain, but not survival, was signif- significantly reduced by 91–100% and 21–45%, respectively.
icantly affected by plant position (P ϭ 0.0418); however, differ- Most larvae died within 1 h of exposure to sprayed leaves. Initial ences across plant positions were not consistent with levels of weights during days 3, 6, and 9 averaged 2.2, 2.2, and 3.5 mg per pollen. This last bioassay used a combination of late-first and larva, respectively. On day 3, the weight gain of surviving larvae early-second instars with an initial weight of 5.6 mg per larva and was significantly influenced by the treatment by position inter- leaves from only four transects of plants. Thus, weight gains were action (P ϭ 0.0003). Larvae fed milkweed leaves collected from significantly higher compared with previous bioassays and ex- inside unsprayed non-Bt plots exhibited the greatest weight gain, whereas those larvae exposed to ␭-cyhalothrin on leaves inside Sweet-corn experiment. Maximum levels of pollen from both Bt sprayed plots did not survive and, thus, showed no weight gain.
and non-Bt hybrids were deposited on milkweeds at 6 to 9 days For bioassays conducted on days 6 and 9 of anthesis, the after the onset of anthesis. Peak levels of pollen on milkweeds treatment by position interaction and main effect for position situated 3 m inside plots averaged 504–586 grains per cm2 and were not significant. On day 6, only the treatment effect was were significantly higher than levels on plants outside plots that significant (P ϭ 0.0045); average weight gains of larvae feeding peaked at 18–22 grains per cm2 (P Ͻ 0.0001). The overall level on milkweeds from Bt plots were significantly higher than those of pollen produced by both hybrids over time was statistically the of larvae feeding on plants from non-Bt plots. The insecticide same. Rain events, recorded on day 5 (2 mm) and day 9 (36 mm) significantly reduced the weight gains of surviving larvae feeding of anthesis, may have removed some pollen.
on plants from both inside and outside the sprayed non-Bt plots.
Data on larval survival and weight gain were analyzed sepa- On day 9, overall weight gains of larvae after 4 days of feeding 11934 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.211277798
typically less diverse in flora and fauna than field edges, and thus larvae may experience less predation within cornfields (13).
DiscussionThese studies provide evidence that the amount of pollen deposited on milkweed leaves and the Cry1Ab expression in pollen largely predict impacts of pollen on monarch larvae feeding on milkweed associated with Bt corn during anthesis. In the Iowa I study, low doses of event-176 pollen averaging 23 grains per cm2 had a significant effect on weights of first instars, although survival differences were not statistically significant.
Results from the field-corn experiment conducted in Maryland show that the survival and growth of first instars were signifi- cantly affected when event-176 pollen levels reached Ϸ67 grains per cm2 of leaf area. Survival of larvae feeding on milkweeds within the field during peak anthesis was reduced by as much as 60%, and weight gain was also reduced by as much as 42% compared with larvae feeding on milkweeds outside of the field.
These results are consistent with those of Jesse and Obrycki (5), who observed a decrease in the survival of larvae exposed to event-176 pollen on leaves from within a field (80–217 pollen grains per cm2) compared with those fed leaves from outside of the field. The results are also consistent with laboratory studies that have shown reductions in weight gain at doses as low as 5–10 grains per cm2 after a 4-day exposure period (8).
In contrast, Mon810 and Bt11 hybrids do not seem to have direct adverse effects on larval survival. The Iowa I study demonstrates that low doses of Mon810 pollen (26 grains per cm2) do not affect survivorship or weight gain of first instars after a 5-day exposure period. The New York study also shows that survival of developing larvae on milkweeds located within the field was not significantly affected after exposure to Mon810 Survival curves for monarch larvae placed in and near Bt and non-Bt pollen for 22 days. These results are not surprising, because corn fields. (a) Iowa. (b) New York.
Mon810 pollen expresses far less toxin than event-176 pollen.
None of the studies show an effect of Bt11 pollen on survivorship or weight gain either outside or inside the field, even where were higher than the previous bioassays because of higher initial pollen densities as high as 586 grains per cm2 of leaf area were weights. A significant treatment effect (P ϭ 0.0148) indicated observed. In the Ontario study, neither first nor third instars that weight gains for the Bt and non-Bt (unsprayed) treatments were detrimentally affected by pollen from event-Bt11 hybrids were the same but significantly higher than average weights of after exposure to pollen densities of 55 and 97 grains per cm2, larvae feeding on milkweed leaves from both inside and outside respectively. The survival, growth, and development of later-life stages were also unaffected at these doses; larvae caged in Bt11 cornfields, non-Bt cornfields, or control areas developed into Iowa II and New York Studies. Pollen densities among the three pupae and adults of similar weight and size within similar sites in Iowa were similar between hybrids and ranged from 154 developmental times. However, the percent of emergence may to 367, 11 to 116, and 5 to 36 grains per cm2 within, at the edge, have been affected by Bt11 pollen and warrants further inves- and 2 m outside the field, respectively. There were no significant tigation. In the Iowa II study, no effects on survival were differences in the numbers of larvae surviving and in the survival observed for larval cohorts feeding for 14 days on milkweed curves among the three field sites. The number of larvae alive plants within Bt11 corn plots with average pollen levels of 241 over the 14 days in the Bt and non-Bt corn plots was statistically grains per cm2. Results from the sweet-corn experiment with the the same. The survival curves of larvae pooled over the three Bt Bt11 event show no effects on monarch survival or growth after corn sites were not significantly different from those in non-Bt 4 days at the three bioassay times during anthesis, compared with (Fig. 4a). In New York, trends in survivorship were also statis- larvae in and near non-Bt plots that were not treated with tically the same for cohorts of larvae feeding for 22 days on insecticide. These field studies are consistent with those of milkweeds in Bt and non-Bt fields (Fig. 4b). Pollen counts on laboratory studies that suggest that exposure to Bt11 pollen at milkweeds in the field averaged 127 grains per cm2 and were not doses of less than 1,000 grains per cm2 do not detrimentally affect significantly different between hybrids. The early-instar larvae first-instar monarchs after a 4-day exposure period (8).
Most of the studies reported herein did not examine expo- may have experienced higher pollen levels because counts were sure in the middle of cornfields where pollen densities may be made 6 days after larvae were introduced and Ͻ24 h after higher than at the plot edge (14). However, in the sweet-corn significant precipitation that may have reduced pollen levels experiment, unaffected larvae fed on milkweed leaves with Ͼ3 (12). For data pooled over hybrids, the survivorship curves in times the pollen densities typically found in field-corn plots. Bt both studies indicated significantly lower survival on milkweeds sweet corn can be viewed as a worst-case scenario corn type for at the edge of the field compared with survival at the other testing nontarget effects because it produces more pollen per locations (Iowa: log-rank test, P Ͻ 0.09; Wilcoxon test, P Ͻ 0.04; plant than field corn and is heavily treated with insecticides New York: log-rank test, P Ͻ 0.009; Wilcoxon test, P Ͻ 0.04).
(http:͞͞www.epa.gov͞scipoly͞sap͞2000͞october͞). Further- The same result has been observed in other studies for non-Bt more, Cry1Ab expression in the pollen of Bt sweet corn is fields and is probably explained by the fact that cornfields are comparable to the expression in field-corn hybrids based on PNAS ͉ October 9, 2001 ͉ vol. 98 ͉ no. 21 ͉ 11935
the Bt11 event. Thus, results of nontarget effects in sweet corn recorded the fate of experimental cohorts of larvae for 14 to 22 can be extrapolated to risk scenarios for field corn.
days and show no apparent effect of Bt11 or Mon810 pollen on The sweet-corn experiment also demonstrates the importance survival, although the presence of other mortality factors con- of assessing the risks of Bt corn to monarch populations in terms tributed to high levels of variability in mortality rates; thus, subtle of the relative risks of other agricultural practices. Monarch effects of prolonged exposure to Bt toxin cannot be determined.
larvae were adversely affected by treatments of ␭-cyhalothrin Further, potential sublethal effects in response to long-term applied to non-Bt plots of sweet corn. Most larvae died within exposure, exposure of neonate larvae, and the potential impact hours after feeding on milkweed leaves collected from plants of Bt pollen on reproductive fitness and migration abilities could exposed within plots to the spray application. Survival and not be determined in these studies. Finally, because the detection growth of larvae feeding on milkweeds outside of the sprayed of very subtle effects is difficult in field studies because of the plots also was reduced because of insecticide drift. These results relatively small sample sizes, the results of these studies must be were not surprising because ␭-cyhalothrin is very effective at considered with the results of much higher doses and more controlling lepidopteran pests, and many reports have docu- rigorous laboratory studies (8). In addition, the implications of mented nontarget effects of conventional insecticides (14).
these studies must be understood in the context of the environ- Recent data suggest that the use of Bt hybrids has the potential mental doses anticipated throughout pollen dispersal (12) and to significantly reduce the number of insecticide treatments the likelihood that monarch larvae will be exposed to toxic doses that are typically applied to sweet corn (http:͞͞www.epa.
gov͞scipoly͞sap͞2000͞october͞).
Differences in overall results of the Iowa I, Ontario, and We thank Laura Timms, Pat Beaupre, Matt Van Ast, Bryan Muscat, Maryland bioassays are clearly attributable to the protein ex- Chad Harvey, Eric Olson, Terry Patton, Jeff Miner, Jessica Nelson, pression level in pollen that is regulated by the transformation Keith Bidne, Randy Ritland, Jim Robbins, Colothdian Tate, Patricia event. Corn hybrids based on event 176 may be hazardous to Anderson, Denny Bruck, Stacy van Loon, Kate Kronback, Jaleen susceptible stages of monarch larvae that are present on their Bruner, Karen Douchette, Kerry Gillooly, Erin Roe, Tegwin Taylor, host plants within cornfields during anthesis. However, the Maureen Carter, Lee Macomber, Jeremiah Depue, Christine Cappa- dora, Jeffrey Fuchsberg, and Christa Hoffman for their assistance in exposure dose of Bt11 pollen present at peak anthesis and the conducting field trials. We also thank Fred Gould, George Kennedy, Cry1Ab concentration in pollen ingested over the 4- or 5-day Kevin Steffey, Anthony Shelton, Jeffrey Wolt, and Eric Sachs for their feeding period was not high enough to significantly affect larval critical reviews and Orley Taylor (Monarch Watch, University of Kansas) survival. These findings are probably true for Mon810 as well, for providing monarch larvae. This research was supported by a pooled although it was not vigorously tested, because Cry1Ab expres- grant provided by the United States Department of Agriculture, Agri- sion in Mon810 is similar to that in Bt11 pollen. However, further cultural Research Service, and the Agricultural Biotechnology Steward- research is required to better understand the impact of Bt pollen ship Technical Committee (ABSTC), and by funding from the Canadian with relatively low toxicity on monarch populations. For exam- Food Inspection Agency, Environment Canada, the Ontario Corn ple, in the natural setting, larvae hatching at the onset of anthesis Growers’ Association, the Maryland Agricultural Experiment Station, and the Leopold Center for Sustainable Agriculture (Ames, IA). Mem- may be exposed to biologically active Cry1Ab in pollen for a bers of ABSTC are Aventis CropScience USA LP, Dow AgroSciences longer period than 4 or 5 days; thus, exposure duration needs to LLC, E. I. du Pont de Nemours and Company, Monsanto Company, and be considered along with exposure concentration as a determi- Syngenta Seeds, Inc. L.C.H.J. was supported by an Environmental nant of environmental dose. The Iowa II and New York studies 1. Koziel, M. G., Beland, G. L., Bowman, C., Carozzi, N. B., Crenshaw, R., 9. Raynor, G. S., Ogden, E. C. & Hayes, J. V. (1972) Agron. J. 64,
Crossland, L., Dawson, J., Desai, N., Hill, M., Kadwell, S., et al. (1993) Biotechnol. 11, 194–200.
10. Russek-Cohen, E. & Douglas, L. W. (1999) Mixed Model Short Course Manual 2. Schuler, T. H., Poppy, G. M., Kerry, B. R. & Denholm, I. (1999) Trends (University of Maryland, Beltsville), pp. 89–103.
Biotechnol. 17, 210–216.
11. SAS Institute (1990) SAS͞STAT User’s Guide, Version 6.0 (SAS Inst., Cary, 3. Fearing, P. L., Brown, D., Vlachos, D., Meghji, M. & Privalle, L. (1997) Mol. Breeding 3, 169–176.
12. Pleasants, J. M., Hellmich, R. L., Dively, G., Sears, M. K., Stanley-Horn, D. E., 4. Losey, J. E., Rayor, L. S. & Carter, M. E. (1999) Nature (London) 399,214.
Mattila, H. R., Foster, J. E., Clark, P. L. & Jones, G. D. (2001) Proc. Natl. Acad. 5. Jesse, L. C. H. &. Obrycki, J. J. (2000) Oecologia 125, 241–248.
Sci. USA 98, 11919–11924. (First Published September 14, 2001; 10.1073͞
6. Malcolm, S. B. & Brower, L. P. (1989) Experientia 45, 284–294.
7. Wassenaar, L. I. & Hobson, K. A. (1998) Proc. Natl. Acad. Sci. USA 95,
13. Oberhauser, K. S., Prysby, M., Mattila, H. R., Stanley-Horn, D. E., Sears, M. K., Dively, G., Olson, E., Pleasants, J. M., Lam, W.-K. F. & Hellmich, R. L. (2001) 8. Hellmich, R. L., Siegfried, B., Sears, M. K., Stanley-Horn, D. E., Daniels, M. J., Proc. Natl. Acad. Sci. USA 98, 11913–11918. (First Published September 14,
Mattila, H. R., Spencer, T., Bidne, K. G. & Lewis, L. (2001) Proc. Natl. Acad. Sci. USA 98, 11925–11930. (First Published September 14, 2001; 10.1073͞
14. Jepson, P. C. (1989) Pesticides and Non-Target Invertebrates (Intercept, An- 11936 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.211277798

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