Field Efficacy of Sweet Corn Hybrids Expressing a Bacillus Thuringiensis

HORTICULTURAL ENTOMOLOGY Field Efﬁcacy of Sweet Corn Hybrids Expressing a Bacillus thuringiensis Toxin for Management of Ostrinia nubilalis (Lepidoptera: Crambidae) and Helicoverpa zea (Lepidoptera: Noctuidae)

ERIC C. BURKNESS,1 W. D. HUTCHISON,1 PATRICIA C. BOLIN,2 DAVID W. BARTELS,3 4 5 D. F. WARNOCK, AND D. W. DAVIS

J. Econ. Entomol. 94(1): 197Ð203 (2001) ABSTRACT Field studies were done in 1995Ð1996 to assess the efÞcacy of three sweet corn hybrids that express the Bacillus thuringiensis (Bt) toxin, Cry1Ab, against two lepidopteran pests, Ostrinia nubilalis (Hu¨ bner) and Helicoverpa zea (Boddie). The Bt hybrids tested were developed by Novartis Seeds, using the event BT-11, which expresses Bt toxin in green tissue as well as reproductive tissues including the tassel, silk, and kernel. Bt hybrids were compared with a standard non-Bt control or the non-Bt isoline for each hybrid; none of the hybrids were treated with insecticides during the study. Hybrid efÞcacy was based on larval control of each pest, as well as plant or ear damage associated with each pest. In both years, control of O. nubilalis larvae in primary ears of all Bt hybrids was 99Ð100% compared with the appropriate non-Bt check. Plant damage was also signiÞcantly reduced in all Bt hybrids. In 1996, control of H. zea in Bt hybrids ranged from 85 to 88% when compared with the appropriate non-Bt control. In 1996, a University of Minnesota experimental non-Bt hybrid (MN2 ϫ MN3) performed as well as the Bt hybrids for control of O. nubilalis. Also, in 1996, two additional University of Minnesota experimental non-Bt hybrids (A684su X MN94 and MN2 ϫ MN3) performed as well as Bt hybrids for percent marketable ears (ears with no damage or larvae). In addition, compared with the non-Bt hybrids, percent marketable ears were signiÞcantly higher for all Bt hybrids and in most cases ranged from 98 to 100%. By comparison, percent marketable ears for the non-Bt hybrids averaged 45.5 and 37.4% in 1995 and 1996, respectively. Results from the 2-yr study strongly suggest that Bt sweet corn hybrids will provide high levels of larval control for growers in both fresh and processing markets. SpeciÞcally, Bt sweet corn hybrids, in the absence of conventional insecticide use, provided excellent control of O. nubilalis, and very good control of H. zea. However, depending on location of speciÞc production regions, and the associated insect pests of sweet corn in each area, some insecticide applications may still be necessary.

KEY WORDS Ostrinia nubilalis, Helicoverpa zea, Bacillus thuringiensis, transgenic sweet corn

CONTROL OF EUROPEAN corn borer, Ostrinia nubilalis ear tip (Flood et al. 1995). Given the larval behavior (Hu¨ bner) and corn earworm, Helicoverpa zea (Bod- of each species, imperfect insecticide coverage, and die), is a major concern for producers of fresh-market limited residual activity of insecticides (Rinkleff et al. and processing sweet corn, Zea mays L., in Minnesota 1995), growers must use multiple applications to (Gingera et al. 1993, Bartels and Hutchison 1995). achieve marketable produce. Until recently, control options have been primarily A novel approach to reducing insecticide use in limited to foliar insecticide applications. Insecticidal sweet corn is the development of transgenic sweet control, however, is often inadequate because of im- corn where a cry gene from Bacillus thuringiensis perfect timing of applications (e.g., Bartels and (Berliner) (Bt) is transferred to the genome of sweet Hutchison 1995). This is primarily due to the rapid corn inbreds to create transgenic Bt hybrids (Ostlie et movement of neonates, soon after egg hatch, into the al. 1997, Lynch et al. 1999a). This transfer of the cry Bt gene allows for the production of Bt toxins in several 1 University of Minnesota, Department of Entomology, 1980 Fol- tissues of the sweet corn plant. Novartis Seeds well Avenue, St. Paul, MN 55108Ð6125. (Nampa, ID) developed the Þrst sweet corn hybrids 2 Oklahoma State University, Integrated Pest Management Pro- using the 35S promoter (Armstrong et al. 1995), and gram, Department of Entomology, Noble Research Center, Stillwater, OK 74078. the gene for Cry1Ab Bt protein (Lynch et al. 1999a). 3 USDA-APHIS-PPQ, Mission Plant Protection Center, Moore Air This event, BT-11, which provides high Bt expression Base, Building S-6414, P.O. Box 2140, Mission, TX 78573. levels in Þeld corn (Ostlie et al. 1997), also provides 4 University of Illinois, Department of Natural Resources and En- high Bt concentrations in green leaf, silk, and kernel vironmental Sciences, 1029 Plant Science Laboratory, MC-634, 1201 South Darner Drive, Urbana, IL 61801. tissue of several sweet corn hybrids (Lynch et al. 5 University of Minnesota, Department of Horticultural Science, 1999a). Lynch et al. (1999a) found that the Novartis 1970 Folwell Avenue, St. Paul, MN 55108Ð6125. sweet corn hybrids Btk-0906, Btk-0907, Btk-0908, and

0022-0493/01/0197Ð0203$02.00/0 ᭧ 2001 Entomological Society of America 198 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 94, no. 1

Btk-0909 provided high levels of control against H. zea portion of each plot and from 14 to 42 primary ears in and fall armyworm, Spodoptera frugiperda (J.E. the naturally infested portion of each plot. Total num- Smith). They showed that a high level of plant resis- ber of O. nubilalis larvae, larval instar, location of tance was evident in leaf and silk tissue for control of larvae and presence of feeding damage were recorded H. zea. Although efÞcacy against S. frugiperda was less for each ear. Presence of larvae and/or feeding dam- striking, these authors concluded that the use of Bt age caused by O. nubilalis on the primary ear was used sweet corn would signiÞcantly reduce conventional to determine the percentage of marketable ears (i.e., insecticide use for both insect pests. percentage of ears without larvae or damage). On 6 The purpose of this study was to document the September, stalk dissections were performed on Þve impact of several BT-11 sweet corn hybrids, expressing arbitrarily selected plants per plot. For each stalk, data Cry1Ab toxin, by comparing them with convention- were recorded for number of tunnels, length of tun- ally bred insect-resistant and susceptible hybrids for nels, and whether the tassel had been broken because control of O. nubilalis and H. zea and their associated of O. nubilalis larval feeding. plant damage. In 1996, plots were also established at the Rose- mount Experiment Station. All sweet corn hybrids were planted 24 June in a randomized complete block Materials and Methods design with four replicates. Plot size was increased Sweet corn plots were established in 1995 and 1996 from 1995 to 4 rows because of an increase in seed at the Rosemount Experiment Station, Rosemount, availability. Rows were nine m long with 76-cm row MN. Each year, O. nubilalis moth ßights were moni- spacing and 3.04-m alleys separated replicates. Plant tored using a blacklight trap and moth population spacing within each row was 30 cm. Because of high dynamics were summarized using a 5-d moving aver- natural O. nubilalis populations in 1996 artiÞcial in- age (e.g., Bartels and Hutchison 1995). Treatments in festations were unnecessary. Hybrids were evaluated 1995 consisted of three sweet corn hybrids expressing 17 September by harvesting 25 primary ears per plot Cry1Ab, a non-Bt hybrid (Apache) produced through and recording total number and ear location of O. conventional breeding with O. nubilalis resistance, nubilalis and H. zea larvae, instar of O. nubilalis larvae, and a standard O. nubilalis susceptible non-Bt hybrid and presence of ear damage. As in 1995, the percent- (Jubilee) (see also Bolin et al. 1996). The 1995 Bt age of marketable ears was recorded. On 20 Septem- hybrids included Rogers-8274, Rogers-8264 and ber, Þve plants were arbitrarily selected from each plot Rogers-8277. In 1996, three improved Bt hybrids were in the Þrst three replicates for stalk dissection. Num- evaluated, reßecting additional backcrosses of the pre- ber of tunnels, length of tunnels, and broken tassels vious hybrid material, but still based on the BT-11 caused by O. nubilalis larval feeding were recorded for event. The Bt hybrids, 95-0937, 95-0941, and 95-0943 each stalk. were compared. The respective O. nubilalis suscepti- Data for each year were analyzed separately using ble non-Bt isolines of Jubilee, Empire, and Heritage a one-way analysis of variance and the Ryan-Einot- were included as non-Bt standards. In addition, the Gabriel-Welsch multiple range test (P ϭ 0.05) for non-Bt hybrid Apache and three experimental Uni- mean separation (SAS Institute 1995). Insect counts versity of Minnesota O. nubilalsis resistant non-Bt hy- were transformed using a square root (͌x ϩ 0.5) and brids (A684su ϫ MN94, MN96 ϫ A685su, and MN2 ϫ data recorded as proportions were transformed using MN3) were included in the 1996 trial. The Minnesota arcsine and square-root transformation (SAS Institute hybrids were developed using lines A684su and 1995). A685su (Davis et al. 1993). No insecticide treatments were made to any of the hybrids during either year of Results the study. In 1995, sweet corn was planted 6 June and plots Initiation of the Þrst-generation O. nubilalis moth were arranged in a randomized complete block design ßight was very similar for 1995 and 1996, with peak with four replicates (see also Bolin et al. 1998). Plots ßight occurring Ϸ22 June (Fig. 1). Phenology of the consisted of single rows 15 m long, separated by 76 cm, second-generation O. nubilalis moth ßight was also with replicates separated by 3.04-m alleys. Plant spac- similar for both years; peak moth ßight occurred Ϸ3 ing was 30 cm. No H. zea data were recorded in 1995 August (Fig. 1). because of low densities. The Þrst eight plants of each In 1995, results for both natural and artiÞcial infes- plot were artiÞcially infested 27 July (late-whorl tations were similar for plant (Table 1) and ear dam- stage) with Ϸ30 O. nubilalis neonates per plant to age (Table 2). Each of the Bt hybrids provided sig- simulate the timing of a Þrst-generation infestation. niÞcant reductions in the mean number of O. nubilalis Because of a high natural infestation, an artiÞcial in- larvae per plant compared with the non-Bt control festation was not needed to simulate second-genera- Jubilee (Table 1). Mean number of tunnels and cu- tion O. nubilalis. Primary ear evaluations were con- mulative length of tunneling per stalk also were re- ducted 1 September. A variable number of ears were duced signiÞcantly in all Bt hybrids compared with harvested from each plot because the plots were single Jubilee. No broken tassels were observed in the Bt rows and there was a variable plant stand in some plots. hybrids compared with 47 and 42% broken tassels in Subsequently, the number of ears harvested ranged the natural and artiÞcially infested Jubilee, respec- from 7 to 11 primary ears in the artiÞcially infested tively. Compared with Jubilee, Apache provided sig- February 2001 BURKNESS ET AL.: EFFICACY OF BT SWEET CORN HYBRIDS 199

Fig. 1. Total (male and female) blacklight trap catches (5-d moving average) of O. nubilalis adults for 1995 (A) and 1996 (B), Rosemount, MN.

niÞcant reductions in the total number of O. nubilalis All Bt hybrids provided a high level of ear protec- larvae per plant and in cumulative tunnel length per tion, with total O. nubilalis larval infestations reduced stalk. However, Apache neither affected the total by 99Ð100%, compared with the non-Bt control Jubi- number of tunnels per stalk nor reduced the percent- lee (Table 2). Control of O. nubilalis was similar for age of broken tassels. both the natural and artiÞcially infested plots (Table

Table 1. Mean O. nubilalis whole-plant evaluations for plant damage (؎SEM) from natural and artiﬁcial infestations in Bt and non-Bt sweet corn hybrids, Rosemount, MN, 1995

Natural infestation ArtiÞcial infestations Cumulative Cumulative a Total % Total % Hybrid Total tunnel Total tunnel O. nubilalis/ broken O. nubilalis/ broken tunnels/stalk length tunnels/stalk length plantb tasselsc plantb tasselsc (cm)/stalk (cm)/stalk Rogers-8274 (Btϩ) 0.05 Ϯ 0.03c 0.00 Ϯ 0.00b 0.00 Ϯ 0.00c 0 Ϯ 0b 0.03 Ϯ 0.03c 0.09 Ϯ 0.09b 0.03 Ϯ 0.03c 0 Ϯ 0b Rogers-8264 (Btϩ) 0.04 Ϯ 0.03c 0.06 Ϯ 0.04b 0.05 Ϯ 0.03c 0 Ϯ 0b 0.03 Ϯ 0.03c 0.00 Ϯ 0.00b 0.00 Ϯ 0.00c 0 Ϯ 0b Rogers-8277 (Btϩ) 0.03 Ϯ 0.02c 0.03 Ϯ 0.03b 0.02 Ϯ 0.02c 0 Ϯ 0b 0.00 Ϯ 0.00c 0.03 Ϯ 0.03b 0.02 Ϯ 0.02c 0 Ϯ 0b Apache (BtϪ) 3.80 Ϯ 0.60b 3.75 Ϯ 0.34a 9.27 Ϯ 0.72b 56 Ϯ 4a 3.06 Ϯ 0.12b 3.78 Ϯ 0.46a 7.48 Ϯ 1.24b 44 Ϯ 8a Jubilee (BtϪ) 6.88 Ϯ 1.26a 5.53 Ϯ 1.02a 15.98 Ϯ 3.60a 47 Ϯ 8a 6.66 Ϯ 1.20a 5.39 Ϯ 0.77a 16.94 Ϯ 0.97a 42 Ϯ 10a

Means within columns followed by the same letter are not signiÞcantly different; Ryan-Einot-Gabriel-Welsch multiple range test (P ϭ 0.05). Data are transformed by square root for insect counts and arcsine for proportions; back-transformed means are presented. a The Apache (BtϪ) hybrid via conventional breeding, is O. nubilalis-resistant; Jubilee (BtϪ)isO. nubilalis-susceptible. b Total O. nubilalis/plant includes all instars (1Ð5) located on primary and secondary ears, and within the stalk of the plant. c Percentage broken tassels indicates the percentage of tassels either missing or broken because of O. nubilalis larval feeding damage. 200 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 94, no. 1

Table 2. Mean O. nubilalis ear infestation and percentage marketable ears (؎SEM) for natural and artiﬁcial infestations in Bt and non-Bt sweet corn hybrids, Rosemount, MN, 1995

Natural infestation ArtiÞcial infestation a Hybrid Total % marketable Total % marketable (% control)b (% control)b O. nubilalis/ear earsc O. nubilalis/ear earsc Rogers-8274 (Btϩ) 0.02 Ϯ 0.01c (99) 99 Ϯ 1a 0.00 Ϯ 0.00c (100) 100 Ϯ 0a Rogers-8264 (Btϩ) 0.01 Ϯ 0.01c (99) 99 Ϯ 1a 0.00 Ϯ 0.00c (100) 100 Ϯ 0a Rogers-8277 (Btϩ) 0.03 Ϯ 0.02c (99) 100 Ϯ 0a 0.00 Ϯ 0.00c (100) 100 Ϯ 0a Apache (BtϪ) 0.99 Ϯ 0.14b (64) 57 Ϯ 6b 1.03 Ϯ 0.19b (59) 66 Ϯ 11b Jubiliee (BtϪ) 2.72 Ϯ 0.17a Ñ 14 Ϯ 7c 2.54 Ϯ 0.55a Ñ 25 Ϯ 5c

2). Marketability of ears was also signiÞcantly higher the presence of some H. zea in the Bt hybrids, all larvae in all Bt hybrids, ranging from 99Ð100%, when com- found in the Bt hybrids were only Þrst and second pared with Jubilee. Apache signiÞcantly reduced O. instars. Percentage of marketable ears for all Bt hy- nubilalis infestations per ear, providing 64 and 59% larval brids was signiÞcantly higher than that of their non-Bt control in natural and artiÞcially infested plots, respec- isolines. However, 95-0941 yielded signiÞcantly fewer tively. Ear marketability was also signiÞcantly higher for marketable ears than the other Bt hybrids and was not Apache, compared with the non-Bt control Jubilee. signiÞcantly different from the non-Bt hybrid Apache. In 1996, total O. nubilalis larvae per plant was sig- Apache, when compared with the standard check Ju- niÞcantly reduced for all Bt hybrids, when compared bilee, provided a signiÞcant reduction in the total with their non-Bt isolines (Table 3). Total number of number of O. nubilalis per ear with 70% control but tunnels per stalk, as well as cumulative tunnel length, provided no control of H. zea. Percentage of market- also were reduced signiÞcantly in the Bt hybrids. Apache provided no signiÞcant reduction in total O. able ears for Apache (68%), however, was signiÞcantly nubilalis, number of tunnels, or cumulative tunnel improved when compared with Jubilee at 10%. Two length. Percentage of broken tassels was not reduced University of Minnesota experimental hybrids, ϫ ϫ signiÞcantly among any treatment comparisons except A684su MN94 and MN2 MN3, when compared for the 95Ð0943 comparison with Heritage. with Jubilee, performed as well as the Bt hybrids with Percentage control of O. nubilalis and H. zea larval 89 and 95% control of O. nubilalis, respectively; mar- infestations in primary ears was signiÞcantly higher for ketability ranged from 95 to 96%, respectively (Table all Bt hybrids compared with their non-Bt isolines 4). With the exception of MN2 ϫ MN3 (67% control (Table 4). Bt hybrids provided 99Ð100% and 85Ð88% of H. zea), the Minnesota hybrids did not provide a control of O. nubilalis and H. zea, respectively. Despite high level of H. zea control overall.

Table 3. Mean O. nubilalis whole-plant evaluations for plant damage (؎SEM) from natural infestations in Bt and non-Bt sweet corn hybrids, Rosemount, MN 1996

Total Cumulative tunnel % broken Hybrida Total tunnels/stalk O. nubilalis/plantb length (cm)/stalk tasselsc 95-0937 (Btϩ) 0.03 Ϯ 0.03b 0.00 Ϯ 0.00b 0.00 Ϯ 0.00b 13 Ϯ 7ab 95-0941 (Btϩ) 0.00 Ϯ 0.00b 0.07 Ϯ 0.07b 0.03 Ϯ 0.03b 0 Ϯ 0b 95-0943 (Btϩ) 0.00 Ϯ 0.00b 0.00 Ϯ 0.00b 0.00 Ϯ 0.00b 0 Ϯ 0b Jubilee (BtϪ) 3.77 Ϯ 0.67a 3.67 Ϯ 0.93a 8.20 Ϯ 2.19a 33 Ϯ 13ab Empire (BtϪ) 2.65 Ϯ 0.59a 2.60 Ϯ 0.42a 4.90 Ϯ 0.72a 27 Ϯ 13ab Heritage (BtϪ) 3.99 Ϯ 0.54a 3.93 Ϯ 1.27a 9.63 Ϯ 3.56a 47 Ϯ 7a Apache (BtϪ) 2.36 Ϯ 0.38a 2.80 Ϯ 0.12a 7.47 Ϯ 1.85a 20 Ϯ 12ab

Means within columns followed by the same letter are not signiÞcantly different; Ryan-Einot-Gabriel-Welsch multiple range test (P ϭ 0.05). Data were transformed by square root for insect counts and arcsine for proportions; back-transformed means are presented. a Bt and non-Bt controls correspond as follows: 95-0937 (Btϩ) to Jubilee (BtϪ, O. nubilalis-susceptible); 95-0941 (Btϩ) to Empire (BtϪ, O. nubilalis-susceptible); 95-0943 (Btϩ) to Heritage (BtϪ, O. nubilalis-susceptible); and Apache (BtϪ, O. nubilalis-resistant) to Jubilee (BtϪ, O. nublalis-susceptible). b Total O. nubilalis/plant includes all instars (1Ð5) located on primary and secondary ears, and within the stalk of the plant. c Percentage broken tassels indicates the percentage of tassels either missing or broken because of O. nubilalis larval feeding damage. February 2001 BURKNESS ET AL.: EFFICACY OF BT SWEET CORN HYBRIDS 201

Table 4. Mean O. nubilalis and H. zea ear infestation and percentage marketable ears (؎SEM) for natural infestations in Bt and non-Bt sweet corn hybrids, Rosemount, MN, 1996

Total Hybrida (% control)b Total H. zea/ear (% control)c % marketable earsd O. nubilalis/ear 95-0937 (Btϩ) 0.02 Ϯ 0.02ef (99) 0.05 Ϯ 0.02c (85) 98 Ϯ 2a 95-0941 (Btϩ) 0.00 Ϯ 0.00f (100) 0.06 Ϯ 0.04c (85) 84 Ϯ 4bc 95-0943 (Btϩ) 0.00 Ϯ 0.00f (100) 0.04 Ϯ 0.02c (88) 99 Ϯ 1a Jubilee (BtϪ) 2.73 Ϯ 0.17a Ñ 0.33 Ϯ 0.05ab Ñ 10 Ϯ 4d Empire (BtϪ) 2.05 Ϯ 0.39a Ñ 0.40 Ϯ 0.06a Ñ 17 Ϯ 8d Heritage (BtϪ) 2.43 Ϯ 0.38a Ñ 0.34 Ϯ 0.05ab Ñ 16 Ϯ 2d Apache (BtϪ) 0.83 Ϯ 0.13b (70) 0.38 Ϯ 0.04a (0) 68 Ϯ 7c A684su ϫ MN 94 (BtϪ) 0.30 Ϯ 0.08cd (89) 0.25 Ϯ 0.07abc (24) 95 Ϯ 1ab MN 96 ϫ A685su (BtϪ) 0.65 Ϯ 0.07bc (76) 0.25 Ϯ 0.11abc (24) 76 Ϯ 7c MN 2 ϫ MN 3 (BtϪ) 0.15 Ϯ 0.06de (95) 0.11 Ϯ 0.04bc (67) 96 Ϯ 2a

Means within columns followed by the same letter are not signiÞcantly different; Ryan-Einot-Gabriel-Welsch multiple range test (P ϭ 0.05). Data were transformed by square root for insect counts and arcsine for proportions; back-transformed means are presented. a Bt and non-Bt controls correspond as follows: 95-0937 (Btϩ) to Jubilee (BtϪ, O. nubilalis-susceptible); 95-0941 (Btϩ) to Empire (BtϪ, O. nubilalis-susceptible); 95-0943 (Btϩ) to Heritage (BtϪ, O. nubilalis-susceptible); and Apache (BtϪ, O. nubilalis-resistant), A684su ϫ MN 94 (BtϪ, O. nubilalis-resistant), MN 96 ϫ A685su (BtϪ, O. nubilalis-resistant), and MN 2 ϫ MN 3 (BtϪ, O. nubilalis-resistant) to Jubilee (BtϪ, O. nubilalis-susceptible). b Total O. nubilalis/ear includes all instars (1Ð5) on the tip, side, or butt of the primary ear; % control determined using the non-Bt isoline for each Bt hybrid. c Total H. zea for Bt hybrids refers to Þrst and second instars only, located on the tip, side, or butt of the primary ear; % control determined as with O. nubilalis. Total H. zea for all non-Bt hybrids includes all instars (1Ð6). d Percentage marketable ears reßects the total number of ears without feeding damage or larvae, divided by the total number of ears harvested (primary ears only).

Discussion was high (i.e., Ͼ0) for one Bt hybrid (95-0937; Table 3) and ear marketability was slightly lower for one Bt The second-generation O. nubilalis moth ßight is hybrid (84%, 95-0941; Table 4). Although percentage usually the most damaging to Minnesota sweet corn of broken tassels was not reduced statistically in the Bt (e.g., Bartels and Hutchison, 1995). In 1995 and 1996, the phenology of the second-generation moth ßight hybrids in 1996, these hybrids continued to incur less was very similar at Rosemount, with the peak ßight damage, ranging from 0 to 13%, compared with 27 to occurring approximately on 3 August (Fig. 1). Silk 42% for the non-Bt isolines (Table 3). Moreover, the initiation for most late-season sweet corn hybrids usu- 13% broken tassel level would likely have little impact ally begins 18Ð21 d before harvest (Flood et al. 1995). on kernel Þll or yield in a commercial-size sweet corn This timing places silk initiation at Ϸ14 August in 1995, Þeld. and Ϸ31 August in 1996. Consequently, the sweet corn In 1996, Bt hybrids provided 85Ð88% control of H. plots should have been very attractive for oviposition zea larvae, with 95-0941 yielding only 84% marketable by O. nubilalis shortly after peak moth ßight occurred. ears (Table 4). Given the fact that O. nubilalis control Indeed, for both years we observed high densities of for this hybrid was 100%, the lower marketability was O. nubilalis larvae/plant, with natural infestations in likely due to the inßuence of H. zea damage. Although the non-Bt hybrid Jubilee ranging from 6.88 to 3.77/ more H. zea larvae may survive on Bt hybrids there are plant, in 1995 and 1996, respectively (Tables 1 and 3). Þtness costs associated with survival. Lynch et al. Unlike the silk date in 1995, the late August silk date (1999a) found that 6-d-old H. zea larvae still surviving in 1996 was more favorable for H. zea oviposition, on Bt sweet corn were generally lethargic, had usually when H. zea moths typically migrate into southern ceased feeding, and had lost weight when compared Minnesota (e.g., Bartels and Hutchison 1995). with average weights at the beginning of the test or During both years of the study, all of the Bt hybrids with larvae that had fed on non-Bt sweet corn. Al- provided a signiÞcant and high level of O. nubilalis though low densities of H. zea were recorded for the control for both ear protection and in minimizing Bt hybrids 95-0937 and 95-0943, percentage of mar- infestations within the stalk or tassel. Perhaps most ketable ears (98Ð99%) was not adversely affected for important to sweet corn producers, is the consistent these hybrids. Moreover, all H. zea found in the Bt level of ear protection against O. nubilalis, ranging hybrids were limited to Þrst or second instars (Table from 99 to 100% control during both years. These 4), which are typically removed early in the process- results are remarkable given the high infestation levels ing plant (via husking and washing equipment) and in the non-Bt control hybrids (Tables 1Ð4) and the thus are rarely a contaminant concern (e.g., Bartels et fact that no foliar insecticides were applied through- al. 1995). The kernel damage in 95-0941 may have out the study. These results were also consistent when resulted from some feeding by late instars that sub- plants were either naturally or artiÞcially infested with sequently died or exited the ear but still affected ear O. nubilalis in 1995. marketability ratings. Two exceptions to the dramatic level of control The performance of the Minnesota hybrid MN2 ϫ occurred in 1996 when the percentage broken tassels MN3, with 95% control of O. nubilalis larvae in the ear 202 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 94, no. 1

(96% marketable ears), would also be acceptable for sota) for assistance with statistical analysis and reviewing an commercial use. However, as an experimental hybrid, early draft of the manuscript. The research was funded by it does not possess all of the agronomic and kernel Novartis Seeds, Incorporated (formerly Rogers Seed Com- qualities required by the processing industry. Thus, pany), and the Minnesota Agricultural Experiment Station, the parental inbreds for this hybrid, as well as the other University of Minnesota, St. Paul, MN. This is publication inbreds used in this study, would likely be most useful 00117-0011 of the Minnesota Agricultural Experiment Sta- tion. to the industry as additional sources of insect resistant germplasm that could be combined with transgenic inbreds to provide new transgenic hybrids with multiple sources of resistance (Davis et al. 1993) versus References Cited hybrids based on single Bt cry genes (e.g., Andow and Andow, D. A., and W. D. Hutchison. 1998. Bt-Corn resis- Hutchison, 1998). tance management, pp. 19Ð66. In M. Mellon and J. Rissler In the current study, the level of O. nubilalis control [eds.], Now or never: serious new plans to save a natural provided by the Bt hybrids and that of the Minnesota pest control. Union of Concerned Scientists, Washington, hybrid MN2 ϫ MN3 is comparable to and often su- DC. perior to that of conventional insecticides (e.g., Bar- Armstrong, C. L., G. B. Parker, J. C. Pershing, S. M. Brown, tels and Hutchison 1995, Rinkleff et al. 1995). The P. R. Sanders, D. R. Duncan, T. Stone, D. A. Dean, D. L. performance of these hybrids for insect control would DeBoer, J. Hart, and others. 1995. Field evaluation of therefore be acceptable for either fresh-market or European corn borer control in progeny of 173 transgenic corn events expressing an insecticidal protein from Ba- processing sweet corn production (Bartels et al. 1995, cillus thuringiensis. Crop Sci. 35: 550Ð557. Bolin et al. 1996). Moreover, in Minnesota, where O. Bartels, D. W., and W. D. Hutchison. 1995. On-farm efÞ- nubilalis is the primary insect pest of sweet corn and cacy of aerially applied Bacillus thuringiensis for Euro- from two to four synthetic insecticide applications are pean corn borer (Lepidoptera: Pyralidae) and corn ear- necessary from late-whorl to harvest to achieve mar- worm (Lepidoptera: Noctuidae) control in sweet corn. J. ketable produce (Noetzel et al. 1985, Gingera et al. Econ. Entomol. 88: 380Ð386. 1993), use of Bt hybrids could eliminate the need for Bartels, D. W., and W. D. Hutchison, V. A. Fritz, and G. R. insecticides to control this pest (e.g., Bartels and Klacan. 1995. Effect of Bacillus thuringiensis application Hutchison 1995). interval on European corn borer (Lepidoptera: Pyrali- In summary, sweet corn hybrids expressing the dae) control in sweet corn. J. Entomol. Sci. 30: 374Ð389. Bolin, P. C., W. D. Hutchison, D. A. Andow, and K. R. Ostlie. Cry1Ab toxin, using the BT-11 event, could be very 1998. Monitoring for European corn borer (Lepidoptera: useful as a foundation for more biologically based Crambidae) resistance to Bacillus thuringiensis: logistical integrated pest management programs in sweet corn constraints when sampling larvae. J. Agric. Entomol. 15: (e.g., Lynch et al. 1999b). Scheduled or calendar spray 231Ð238. regimes are often used once lepidopteran pest pres- Bolin, P. C., W. D. Hutchison, and D. W. Davis. 1996. Re- sure is Þrst detected in sweet corn (Flood et al. 1995, sistant hybrids and Bacillus thuringiensis for management Lynch et al. 1999b). For pests such as H. zea and S. of European corn borer (Lepidoptera: Pyralidae) in frugiperda, which may not be as effectively controlled sweet corn. J. Econ. Entomol. 89: 82Ð91. by Cry1Ab, Bt hybrids will still aid in reducing insec- Davis, D. W., D. A. Andow, and W. D. Hutchison. 1993. Registration of three European corn borer resistant sweet ticide applications (Lynch et al. 1999b). For H. zea in corn germplasm lines: A684su, A685su, A686su. Crop Sci. the upper Midwestern United States, insecticide use 33: 1451Ð1457. should typically be limited to only one late-season Flood, B., R. Foster, and B. Hutchison. 1995. Sweet corn, pp. application, for protection of late-planted sweet corn. 19Ð40. In R. Foster and B. Flood [eds.], Vegetable insect With less conventional insecticide use, Bt sweet corn management: with emphasis on the Midwest. Meister, hybrids should also prove useful for implementing Willoughby, OH. complementary control tactics such as biological con- Gingera, G. J., B. Subramanyam, and W. D. Hutchison. 1993. trol. However, the use of Bt hybrids with and without Insecticides used by Minnesota processors to control Eu- selective insecticide applications needs to be investi- ropean corn borer and corn earworm in sweet corn. gated further to better understand the full impact of FO-6322-B. Minnesota Extension Service, University of Minnesota, St. Paul, MN. such a strategy, particularly given the possibility that Lynch, R. E., B. R. Wiseman, D. Plaisted, and D. Warnick. new insect pests may emerge (e.g., Ostlie et al. 1997, 1999a. Evaluation of transgenic sweet corn hybrids ex- OÕRourke and Hutchison 2000). Also, the potential of pressing CryIA(b) toxin for resistance to corn earworm insects developing resistance to Bt technology must be and fall armyworm (Lepidoptera: Noctuidae). J. Econ. considered if the market penetration of Bt corn, pri- Entomol. 92: 246Ð252. marily Bt Þeld corn, continues to remain strong or Lynch, R. E., B. R. Wiseman, H. R. Sumner, D. Plaisted, and increase (Andow and Hutchison 1998). D. Warnick. 1999b. Management of corn earworm and fall armyworm (Lepidoptera: Noctuidae) injury on a sweet corn hybrid expressing a cryIA(b) gene. J. Econ. Acknowledgments Entomol. 92: 1217Ð1222. Noetzel, D. M., L. K. Cutkomp, and P. K. Harein. 1985. We thank Sandy Bird, Laurie Cooper, Kelley Dingmann, Estimated annual losses due to insects in Minnesota 1981Ð Becky Hines, Brady Lenzen, Andrew Miller, and Patrick 1983. Univ. Minn. Ext. Serv. Bull. AG-BU-2541. OÕRourke (University of Minnesota) for assistance in the O’Rourke, P. K., and W. D. Hutchison. 2000. First report of Þeld. We also thank Robert Venette (University of Minne- the western bean cutworm, Richia albicosta (Smith) February 2001 BURKNESS ET AL.: EFFICACY OF BT SWEET CORN HYBRIDS 203

(Lepidoptera: Noctuidae), in Minnesota. J. Agric. Urban pean corn borer (Lepidoptera: Pyralidae): ovicidal ac- Entomol. (in press). tivity and residual mortality to neonates. J. Econ. Ento- Ostlie, K. R., W. D. Hutchison, and R. L. Hellmich [eds]. mol. 88: 246Ð253. 1997. Bt corn and European corn borer: long-term suc- SAS Institute. 1995. SAS/STAT userÕs guide, version 6, 4th cess through resistance management. NCR Publication ed. SAS Institute, Cary, NC. 602. University of Minnesota, St. Paul, MN. Rinkleff, J. H., W. D. Hutchison, C. D. Campbell, P. C. Bolin, Received for publication 16 March 2000; accepted 5 October and D. W. Bartels. 1995. Insecticide toxicity in Euro- 2000.