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Assessment of Bt on non-target 249

SHORT-TERM ASSESSMENT OF Bt MAIZE ON NON-TARGET ARTHROPODS IN

Odair Aparecido Fernandes1*; Marcos Faria2; Samuel Martinelli3; Francisco Schmidt2; Vinícius Ferreira Carvalho4; Gloverson Moro5

1 UNESP/FCAV, Depto. de Fitossanidade, Via de acesso Prof. Paulo Donato Castellane, s/n - 14884-900 Jaboticabal, SP - Brasil. 2 Embrapa Recursos Genéticos e Biotecnologia, Parque Estação Biológica, Av. W5 Norte - 70770-900 - Brasília, DF - Brasil. 3 USP/ESALQ - Programa de Pós-Graduação em Entomologia, C.P. 9 - 13418-900 - Piracicaba, SP - Brasil. 4 Conselho de Informações sobre Biotecnologia - CIB, R. André Ampére, 34 - Unidade 12, Brooklin - 04562-080 - São Paulo, SP - Brasil. 5 Syngenta Seeds Ltda., Rod. BR 452 - km 142, C.P. 585 - 38400-974 - Uberlândia, MG - Brasil. *Corresponding author

ABSTRACT: Although not yet available for cultivation in Brazil, the effect of Bt maize hybrids on natural enemies and dwelling arthropods should be assessed prior to its release to growers. Trials were carried out during one growing in two different locations with the genetically modified maize hybrids 7590-Bt11 and Avant-ICP4, comparing with their respective non-Bt isogenic hybrids. Arthropods were evaluated through direct observation on plants and pitfall traps. In general, no differences were observed between populations of earwig (Dermaptera: Forficulidae), lady beetles (Coleptera: Coccinellidae), minute pirate bug (Coleoptera: ), ground beetles (Carabidae), tiger beetles (Cicindelidae), and spiders (Araneae). There was no difference in of (Boddie) by Trichogramma sp. (Hymenoptera: Trichogrammatidae). Thus, Bt maize hybrids expressing Cry1A(b) and VIP 3A do not cause reduction of the main maize dweeling predators and . Key words: Spodoptera frugiperda, Helicoverpa zea, genetically modified crop, maize pests, soil dwelling arthropods

AVALIAÇÃO DO EFEITO DE MILHO Bt SOBRE ARTRÓPODOS NÃO ALVO NO BRASIL

RESUMO: Embora não haja cultivos comerciais de milho geneticamente modificado no Brasil, o efeito de híbridos de milho Bt sobre inimigos naturais e artrópodos de solo deve ser avaliado antes da liberação aos produtores. Assim, ensaios foram conduzidos durante uma safra em duas localidades. Os híbridos de milho modificado geneticamente 7590-Bt11 e Avant-ICP4 foram comparados com seus respectivos isogênicos não transgênicos. Os artrópodes foram avaliados através de observação direta nas plantas e armadilhas de alçapão. De modo geral, não se observaram diferenças entre as populações de tesourinha (Dermaptera: Forficulidae), joaninhas (Coleptera: Coccinellidae), percevejo-pirata (Coleoptera: Anthocoridae), carabídeos (Carabidae), cicindelídeos (Cicindelidae) e aranhas (Araneae). Também não houve diferença no parasitismo de ovos de Helicoverpa zea (Boddie) por Trichogramma sp. (Hymenoptera: Trichogrammatidae). Assim, milho geneticamente modificado expressando as proteínas inseticidas Cry1A(b) e VIP 3A não causa redução nas populações dos principais predadores e parasitóides. Palavras-chave: Spodoptera frugiperda, Helicoverpa zea, cultura geneticamente modificada, pragas do milho, artrópodes de solo

INTRODUCTION has made possible the efficient and specific control of certain lepidopterous pests (Buntin et al., 2001; Stewart Genetically modified (GM) plants resistant to et al., 2001; Wu et al., 2003; Kumar & Kumar, 2004). through the expression of Although already commercially available in several Berliner bacterial toxins (Bt) are considered a new countries (Nap et al., 2003), the use of both Bt management alternative for farmers. This technology and maize in Brazil is currently restricted to experi-

Sci. Agric. (Piracicaba, Braz.), v.64, n.3, p.249-255, May/June 2007 250 Fernandes et al. mental areas (Fontes, 2003). Thus, studies that assess from B. thuringiensis var. kurstaki expressing the in- not only the agronomic efficacy, but also the effects secticide proteins Cry1A(b) and VIP 3A (Estruch et al., of GM plants on natural enemies and other non-target 1996), respectively with toxic properties for certain arthropods associated with GM crops are needed of . The genetically modified ver- (Conner et al., 2003). sions of the inbreds used to produce the GM hybrids Egg parasitoids and predators of maize pests are the result of four generations of backcrosses fol- were not negatively affected by Bt maize expressing lowed by two generations of self-pollinations (BC4S2). Cry1A(b) (Orr & Landis, 1997; Pilcher et al., These BC4S2 versions were selected for 1997; Zwahlen et al., 2000; Al-Deeb et al., 2001). homozigousity of the transgenic trait, as well as, phe- When fed with prey tolerant to the Cry1A(b) toxin, the notypic similarity to their original progenitors. mortality and development of the predator Chrysoperla Crop Management - Soil tillage and other crop man- carnea (Stephens) were not affected (Hilbeck et al., agement practices were performed following the tech- 1998a). On the other hand, Hilbeck et al. (1998b) ob- nical recommendation for maize (Fancelli & Dourado served that a high dose of the Cry1A(b) protein incor- Neto, 2000), using non-treated seeds. Crops were sown porated into an artificial solid diet provided to C. on December 18 1999 (Borborema) and December 3 carnea larvae caused significantly greater mortality 1999 (Uberlândia) using 0.75 to 0.80 m spacing be- than the control. Romeis et al. (2004) showed that the tween rows and six seeds per row meter. As a bio- Cry1A(b) toxin had no direct effect on C. carnea. safety measure, the experimental plots containing GM These authors argued that earlier reported negative ef- plants were detasseled (biosafety mandatory procedure) fects of Bt maize on these predators were due to prey to prevent pollen dispersion from the genetically modi- quality mediated effects rather than to the direct effects fied plants in the study area. The plots with Bt maize of the toxin. plants had two rows of plants from the respective To date, studies to determine the effect of GM isogenic non-Bt cultivar to provide pollen and assure plants on non-target organisms in tropical areas, thus further production. with greater biodiversity, have been rare (O’Callaghan et al., 2005, for review). Thus, the objective of this Experimental Design - The statistical design consisted study was to evaluate the effects of two genetically of randomized complete blocks (RCB) with four treat- modified hybrids expressing B. thuringiensis insecti- ments and three replications. Each experimental unit cide proteins and their isogenic non-transgenic hybrids was 40 m long by 15 rows wide. Three rows of the on herbivore natural enemies that occur in the Brazil- non-GM maize were kept as lateral border around the ian maize agroecosystem. experimental area. In Uberlândia, the isogenic non-Bt of the Bt11 maize had only two replications. MATERIAL AND METHODS Evaluation of Non-target Arthropods - Evaluations th Experiment Location - The experiments were con- were made weekly, beginning on the 4 week after th th ducted in Borborema, SP, Brazil, (21º36’S, 49º02’W) planting (4 WAP) and ending on the 16 WAP th and Uberlândia, MG, Brasil, (18º56’S, 48º10’W) and (Borborema) or 17 WAP (Uberlândia). Predator oc- were duly authorized by the Comissão Técnica currence was evaluated on ten consecutive plants per Nacional de Biossegurança (CTNBio, National Tech- sampling site. Three randomly chosen sites were evalu- nical Biosafety Commission), under proceedings no. ated in each plot, totaling 30 plants per plot. In the 01200.002643/99-17 and 01200.002642/99-54, respec- plots containing Bt maize, the rows of plants provid- tively. Both sites are located in the southeastern region ing pollen were not considered for sampling. The tar- of Brazil ca. 350 km apart. Borborema is located closer get arthropods in this evaluation were the main preda- to a maize growing area but has a greater diversity of tors and parasitoids present in the maize system: ear- crops. Citrus, pasture, coffee, sugarcane and wig adults and nymphs, predator hemipterans, lady are also grown in the municipality. On the other hand, beetles, spiders, and Trichogramma spp. All predators Uberlândia is located in one of the most important but earwig nymphs were counted on each plant. For earwig nymphs, the presence/absence on the plants was maize growing regions of Brazil. Thus, the diversity considered, regardless the number of insects. Parasit- of crops in the region is much lower. ism by Trichogramma was assessed through observa- Genetically Modified Organisms - Treatments in- tion of parasitized Helicoperva zea (Boddie) as cluded the maize hybrids GM 7590-Bt11 and Avant- suggested by Paron et al. (1998). ICP4 and their respective non-Bt isogenic hybrids. The A survey of natural enemies that occur in the hybrids from events Bt11 and ICP4 have genes isolated soil was conducted using pitfall traps, made of 500 mL

Sci. Agric. (Piracicaba, Braz.), v.64, n.3, p.249-255, May/June 2007 Assessment of Bt maize on non-target arthropods 251 plastic bottles buried in the soil surface layer. Five traps not made because they had different phenotypes. More- were randomly placed in each plot. Each trap received over, the results between the two experimental locations 200 mL of 70% ethanol to preserve the trapped insects. were not compared. Bartlett’s test was used to evaluate The traps were installed on the 11th and 15th WAP at the homogeneity of the variance. Transformation was Borborema and on the 10th WAP at Uberlândia and necessary to normalize the data and stabilize the vari- kept in the field for seven days. ance. Statistical analyses were performed using PROC GLM (SAS Institute, 1999). Statistical Analyses - The number of natural enemies per plant and the percentage of plants with earwig RESULTS nymphs at each sampling site were used for the calcu- lation of averages in each experimental plot. The aver- No differences were observed between the Bt ages of natural enemies were transformed to x + 0.5 and hybrids and their respective isogenic non-Bt genotypes used in the analysis of variance. The percentage of para- regarding the average number of earwig, Doru luteipes sitism values were computed as described above and (Scudder), adults per ten plants throughout the crop transformed to arc sine % /100 + 0.5. Data were sub- cycle (Figure 1). The estimate of the orthogonal con- mitted to analysis of variance in a randomized complete trasts showed no difference between the maize hybrids block design with repeated measures. The plots were and their respective non-Bt isogenic for the percent- treatments and the weeks after planting were the sub age of plants with presence of nymphs (Table 1), al- plots. In this way, it was possible to estimate the inter- though minor differences were observed between action between treatments and weeks after planting. maize genetic backgrounds (Group 7590 versus Group Data were estimated for the missing plot at Uberlândia. Avant) at the Uberlândia site. The results of the number of insects collected in the pit- There was no difference in the number of fall traps were also transformed to x + 0.5 and an analy- predator hemipterans occurring on 7590-Bt11 and 7590 sis of variance was conducted in a randomized complete hybrids at Borborema (P = 0.23) and Uberlândia block design. In the occasions when the F test for treat- (P = 0.99). However, there were more predator hemi- ments was significant, the hybrids were compared us- pterans on the Avant-ICP4 hybrid than on its non-ge- ing orthogonal contrast estimates. Thus, the conven- netically modified version at Borborema (P = 0.0394). tional hybrid group was compared with its respective At Uberlândia, no difference between these two hy- GM counterparts, Bt11 and ICP4. However, a compari- brids was observed (P = 0.28) (Table 2). The hemi- son between the hybrids expressing different toxins was pterans found belonged to several families, mainly

30 30 A 7590 A Avant 25 25 7590-Bt11 Avant-ICP4 20 20

15 15 10 10 5 5 Adults/10 plants (+SEM) plants Adults/10 0 Adults/10 plants (+SEM) 0 4 5 6 7 8 9 10 11 12 13 14 15 16 45678910111213141516 Weeks after planting Weeks after planting

30 30 B 7590 B Avant 25 25 7590-Bt11 Avant-ICP4 20 20

15 15

10 10

5 5 Adults/10 plants (+SEM) plants Adults/10 0 (+SEM) plants Adults/10 0 4 5 6 7 8 9 10 11 12 13 14 15 16 17 4 5 6 7 8 9 10 11 12 13 14 15 16 17 Weeks after planting Weeks after planting

Figure 1- Mean density of Doru luteipes (Dermaptera: Forficulidae) adults per ten plants of genetically modified maize and isogenic non-Bt maize throughout the growing season at Borborema, SP (A) and Uberlândia, MG (B).

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Table 1 - Percent1 (±SEM) of maize plants with presence of Doru luteipes nymphs and the estimated orthogonal contrasts. MPaize Hybrids BGorborema, S Uberlândia, M 7590 63.52 ± 4.08 56.33 ± 7.03 74590-Bt11 676.48 ± 4.2 60.67 ± 5.1 Avant 67.78 ± 3.73 53.56 ± 5.75 A6vant-ICP4 705.74 ± 3.3 52.33 ± 5.0 Contrasts P G6roup 7590 vs Group Avant 04.024 0.008 7590-Bt11 vs 7590 0.4425 0.5864 A8vant-ICP4 vs Avant 08.069 0.491

1Original values are shown but they were transformed to arcsine %/100 + 0.5 for statistical analysis.

Table 2 - Average number1 (±SEM) of adult predator hemipterans, lady beetles, and spiders per ten plants and the estimated orthogonal contrasts. Asrthropod Group MPaize Hybrid BGorborema, S Uberlândia, M Predator hemipterans 7590 0.470 ± 0.103 0.048 ± 0.029 74590-Bt11 01.385 ± 0.09 0.071 ± 0.02 Avant 0.709 ± 0.179 0.151 ± 0.034 A6vant-ICP4 03.880 ± 0.17 0.222 ± 0.04 Contrasts P G6roup 7590 vs Group Avant 03.000 0.024 7590-Bt11 vs 7590 0.2332 0.9900 A4vant-ICP4 vs Avant 00.039 0.280 Lady beetles 7590 0.333 ± 0.074 0.036 ± 0.020 71590-Bt11 01.479 ± 0.10 0.048 ± 0.02 Avant 0.718 ± 0.217 0.032 ± 0.016 A7vant-ICP4 03.692 ± 0.14 0.056 ± 0.02 Contrasts P G8roup 7590 vs Group Avant 05.035 0.907 7590-Bt11 vs 7590 0.3313 0.9634 A8vant-ICP4 vs Avant 06.923 0.476 Spiders 7590 0.376 ± 0.097 0.012 ± 0.012 79590-Bt11 05.393 ± 0.08 0.032 ± 0.01 Avant 0.376 ± 0.068 0.079 ± 0.037 A6vant-ICP4 09.718 ± 0.15 0.048 ± 0.01 Contrasts P G1roup 7590 vs Group Avant 06.002 0.349 7590-Bt11 vs 7590 0.5644 0.7881 A6vant-ICP4 vs Avant 05.000 0.611 1Original values are shown but they were transformed to x + 0.5 for the statistical analysis.

Reduviidae, Anthocoridae, Lygaeidae, and were at least 4- and 9-fold higher in Borborema than Pentatomidae. The pirate bug (Say) in Uberlândia, respectively. In Borborema, there were was the predominant species in Borborema, while in more spiders (P = 0.0006) in the Avant-ICP4 hybrid Uberlândia predator hemipterans occurred at low den- than in the isogenic non-Bt hybrid (Table 2). sities and no dominant species was detected. There was no difference between the maize Regarding lady beetles and spiders, the aver- hybrids (P = 0.42 for GM 7590 Bt11 vs. its isogenic age density of predators was less than 0.08 per plant non-Bt and P = 0.60 for Avant-ICP4 vs. its non-Bt) (Table 2). The population of Coccinellidae and Aranae in percentage of parasitism of H. zea eggs by

Sci. Agric. (Piracicaba, Braz.), v.64, n.3, p.249-255, May/June 2007 Assessment of Bt maize on non-target arthropods 253

Trichogramma sp. at the Borborema location (Table 3). respectively. Parasitism of H. zea eggs was not evalu- The average rate of parasitism was always greater than ated at Uberlândia. 29%. At Borborema, 1.31 viable egg of H. zea per At Borborema, in the first evaluation of preda- plant were found on Avant-ICP4, while 0.53 egg per tors collected in the pitfall traps, there was a differ- plant was observed on its non-Bt isogenic. An aver- ence (P = 0.0018) between the treatments Avant and age of 0.24 and 0.50 egg per plant were observed on Avant-IPC4 for the number of rover beetles (Table 4). the 7590-Bt11 hybrid plants and its non-Bt isogenic, In the second evaluation, there was no difference be- tween the treatments for any of the evaluated predator Table 3 - Average percentage of parasitism (±SEM) of arthropods (Table 4). At the Uberlândia location there Helicoverpa zea eggs in Borborema, SP. was no difference in predator arthropods between the Parasitism of H. zea Maize Hybrids Bt hybrids and their isogenic non-Bt hybrids (Table 4). eggs (%)1 Overall, both Borborema and Uberlândia presented no 7590 31.14 ± 10.91 differences in population densities between the treat- 74590-Bt11 29.35 ± 6.0 ments for tiger beetles (Cicindelidae), ground beetles Avant 36.58 ± 11.08 (Carabidae), earwigs (Forficulidae), rover beetles A4vant-ICP4 32.40 ± 9.2 (Staphilinidae) and spiders (Aranae) collected in pit- Contrasts P fall traps. Tiger beetles were not observed at the Uberlândia plots. G3roup 7590 vs Group Avant 0.939 7590-Bt11 vs 7590 0.4243 DISCUSSION A2vant-ICP4 vs Avant 0.596 1Original values are shown but they were transformed to arcsine In general, the Bt maize hybrids did not affect %/100 + 0.5 for the statistical analysis. the D. luteipes population dynamics and other biologi-

Table 4- Average number of predators (±SEM) in pitfall traps and the estimated orthogonal contrasts. Group1 Lgocation Ssamplin Maize Hybrid Ceicindelidae Cearabida Setaphilinida Feorficulida Aranea Borborema, 1 7590 1.75 ± 0.27 0.93 ± 0.41 4.20 ± 1.17 0.07 ± 0.07 1.17 ± 0.38 SP 73590-Bt11 44.07 ± 0.9 11.07 ± 0.2 23.47 ± 1.0 02.13 ± 0.1 1.00 ± 0.1 Avant 2.18 ± 0.72 2.70 ± 0.70 17.87 ± 1.30 0.00 ± 0.00 0.17 ± 0.17 A7vant-ICP4 18.73 ± 0.2 25.15 ± 0.1 58.45 ± 1.8 08.15 ± 0.0 0.85 ± 0.0 Contrasts P G-7roup 7590 vs Group Avant 03.001 0--.001 7590-Bt11 vs 7590 - 0.5909 0.2476 - - A-3vant-ICP4 vs Avant 08.316 0--.001 2 7590 0.45 ± 0.23 0.08 ± 0.08 3.38 ± 0.71 0.27 ± 0.18 0.27 ± 0.13 75590-Bt11 08.93± 0.3 09.47 ± 0.1 22.53 ± 0.6 08.20 ± 0.1 0.47 ± 0.1 Avant 0.15 ± 0.08 0.17 ± 0.17 7.80 ± 3.11 0.07 ± 0.07 0.40 ± 0.23 A0vant-ICP4 02.00 ± 0.0 09.22 ± 0.0 42.82 ± 1.7 09.22 ± 0.0 0.42 ± 0.1 Uberlândia, 1 7590 0.70 ± 0.30 0.10 ± 0.10 0.30 ± 0.10 0.70 ± 0.10 MG 78590-Bt11 05.33 ± 0.1 01.73 ± 0.5 07.40 ± 0.3 0.27 ± 0.0 Avant 1.27 ± 0.27 0.73 ± 0.47 0.93 ± 0.64 0.53 ± 0.29 A4vant-ICP4 20.93 ± 0.8 19.20 ± 0.4 08.47 ± 0.2 0.47 ± 0.1 Contrasts P G-7roup 7590 vs Group Avant 0--.020 7590-Bt11 vs 7590 - 0.5709 - - A-8vant-ICP4 vs Avant 0--.081 1Original values are shown but they were transformed to x + 0.5 for the statistical analysis.

Sci. Agric. (Piracicaba, Braz.), v.64, n.3, p.249-255, May/June 2007 254 Fernandes et al. cal control agents, despite the fact of a reduction in portance, such as aphids and thrips that occurred in the population densities of lepidopteran pests (Martinelli, experimental areas (unpublished data), may contribute 2001). to the population stability of predators and parasitoids, Earwigs, the primary natural enemies of lepi- when there are lower populations of the target lepi- dopteran larvae occurring on maize in Brazil (Cruz & dopteran pests that attack maize hybrids. Oliveira, 1997), were the most frequent predators on Raps et al. (2001) detected that the bird cherry- plants during all phenological stages of the crop. The oat aphid, Rophalosiphum padi (L.), an important prey densities observed for this were greater than the for beneficial insects, contained very low concentra- other natural enemies that occur in maize. Eggs, small tions, or, in many cases, no Cry1A(b) toxin in their larvae (1st and 2nd ) of both fall armyworm, bodies or in their honeydew. Generally, in this study Spodoptera frugiperda (J.E. Smith), and corn earworm, we found a great diversity despite the low density of H. zea, and aphid nymphs are important components of arthropods per plant observed in all treatments. Other the D. luteipes diet (Reis et al., 1988). Even with a lower crops in the neighborhood may have contributed to the availability of Lepidoptera larvae, occurrence of D. observed diversity of insect groups. In Borborema, the luteipes was not impacted in GM plots. maize crop was surrounded by citrus, coffee, sugar- There was no difference in the occurrence of cane, , and pasture, while in Uberlândia, lady beetles, both in Borborema and Uberlândia. The where generally a lower abundance of natural enemies absence of adverse effects of the Bt maize hybrids on was observed, there were only plantings of maize and adult Coccinellidae was also observed in field and soybeans in the neighboring fields. Evaluation of larger laboratory studies by Pilcher et al. (1997). In their areas than the ones used in this experiment may con- tribute to a better understanding of the real effect of study conducted for two consecutive years, no differ- transgenic plants on the food network. In the present ence occurred on non-transgenic and Bt hybrids in the study, parasitoids other than Trichogramma were not number of several Coccinellidae species. Likewise, observed in the experimental areas. there was no difference in the occurrence of predatory Overall, the evidence collected throughout the hemipterans, on Bt and non-Bt hybrids in Borborema production cycle of maize in Borborema and and Uberlândia, although the Avant-ICP4 maize hybrid Uberlândia indicated that the use of Bt maize did not presented a higher density of such predators at the impact populations of non-target arthropods. former location. Similarly, experiments conducted in the laboratory showed that keeping nymphs of O. ACKNOWLEDGEMENT insidiosus with maize Bt pollen did not affect insect survival (Pilcher et al., 1997). Al-Deeb et al. (2001) To Dr. Robert Peterson, Montana State Univer- and Al-Deeb & Wilde (2003) also did not find a sig- sity, for critically reviewing the manuscript. nificant difference in the number of adults and nymphs of O. insidiosus in fields of Bt maize and non-geneti- REFERENCES cally modified maize. Hemipterans belonging to the genus Orius consume small lepidopteran larvae, thrips AL-DEEB, M.A.; WILDE, G.E. Effect of corn expressing the Cry3Bb1 toxin for corn rootworm control on aboveground nontarget (Flint & Dreistadt 1998), and pollen (Orr & Landis arthropods. Biological Control, v.32, p.1164-1170, 2003. 1997). During this research, thrips were detected AL-DEEB, M.A.; WILDE, G.E.; HIGGINS, RA. No effect of Bacillus throughout the developing cycle of the maize plants thuringiensis corn and Bacillus thuringiensis on the predator Orius insidiosus. Environmental Entomology, v.30, p.624-629, in all treatments. Supporting this interaction between 2001. thrips and Orius sp, no adverse effect was detected for BUNTIN, G.D.; LEE, R.D.; WILSON, D.M.; McPHERSON, R.M. the feeding of O. majusculus with thrips that had de- Evaluation of yieldgard resistance for fall armyworm and corn earworm (Lepidoptera: ) on corn. Florida Entomologist, veloped on maize plants expressing the Cry1A(b) pro- v.84, p.38-42, 2001. tein (Zawhlen et al., 2000). CONNER, A.J.; GLARE, T.R.; NAP, J.P. The release of genetically Spiders and other generalist predator occur- modified crops into the environment. Part II. Overview of ecological risk assessment. The Plant Journal, v.33, p.19-46, 2003. rence was not affected by Bt maize plants either. Para- CRUZ, I.; OLIVEIRA, A.C. Flutuação populacional do predador Doru sitism of H. zea eggs by Trichogramma sp. was also luteipes Scudder em plantas de milho. Pesquisa Agropecuária not affected, suggesting that the foraging behavior of Brasileira, v.32, p.363-368, 1997. ESTRUCH, J.J.; WARREN, G.W.; MULLINS, M.A.; NYE, G.J.; females was not hampered by Bt plants. The observed CRAIG, J.A.; KOZIEL, M.G. VIP3A, a novel Bacillus thuringiensis data support a field study conducted by Orr & Landis vegetative insecticidal protein with a wide spectrum of activities (1997) in which the parasitism rate of egg masses of against lepidopteran insects. Proceedings of the National Academy of Sciences of the USA, v.93, p.5389-5394, 1996. O. nubilalis in Bt maize growing areas was not re- FANCELLI, A.L.; DOURADO NETO, D. Produção de milho. Guaiba: duced. Herbivore insects considered of secondary im- Agropecuária, 2000. 360p.

Sci. Agric. (Piracicaba, Braz.), v.64, n.3, p.249-255, May/June 2007 Assessment of Bt maize on non-target arthropods 255

FLINT, M.L.; DREISDADT, S.H. Natural enemies handbook: The PILCHER, C.D.; OBRYCKI, J.J.; RICE, M.E.; LEWIS, L.C. Preimaginal illustrated guide to biological control. Berkeley: University of development, survival and field abundance of insect predators of California Press, 1998.154p. transgenic Bacillus thuringiensis corn. Environmental Entomology, FONTES, E.M.G. Legal and regulatory concerns about transgenic plants v.26, p.446-454, 1997. in Brazil. Journal of Invertebrate Pathology, v.83, p.100-103. RAPS, A.; KEHR, J.; GUGERLI, P.; MOAR, W.J.; BIGLER, F.; 2003. HILBECK, A. Immunological analysis of phloem sap of Bacillus HILBECK, A.; BAUMGARTNER, M.; FRIED, P.M.; BIGLER, F. thuringiensis corn and of nontarget herbivore Rhopalosiphum padi Effects of Bacillus thuringiensis corn-fed prey on mortality and (Homoptera: Aphididae) for the presence of Cry1Ab. Molecular development time of immature Chrysoperla carnea (Neuroptera: , v.10, p.525-533, 2001. Chrysopidae). Environmental Entomology, v.27, p.480-487, 1998a. REIS, L.L.; OLIVEIRA, L.J.; CRUZ, I. Biologia e potencial de Doru HILBECK, A.; MOAR, W.J.; PUSZTAI-CAREY, M.; FILIPPINI, A.; luteipes no controle de Spodoptera frugiperda. Pesquisa BIGLER, F. Toxicity of Bacillus thuringiensis Cry1Ab toxin to the Agropecuária Brasileira, v.23, p.333-342, 1988. predator Chrysoperla carnea (Neuroptera: Chrysopidae). ROMEIS, J.; DUTTON, A.; BIGLER, F. Bacillus thuringiensis toxin Environmental Entomology, v.27, p.1255-1263, 1998b. (Cry1Ab) has no direct effect on larvae of the green lacewing KUMAR, H.; KUMAR, V. expressing Cry1A(b) insecticidal Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). Journal protein from Bacillus thuringiensis protected against tomato fruit of Insect , v.50, p.175-183, 2004. borer, (Hübner) (Lepidoptera: Noctuidae) SAS INSTITUTE. SAS onlinedoc: version 8. Cary, NC.: SAS Institute, damage in the laboratory, greenhouse and field. Crop Protection, 1999. v.23, p.135-139, 2004. STEWART, S.D.; ADAMCZYK, J.R.; KNIGHTEN, K.S.; DAVIS, F.M. MARTINELLI, S. Efeito de híbridos de milho Bt expressando toxinas Impact of Bt expressing one or two insecticidal proteins of de Bacillus thuringiensis Berliner sobre insetos herbívoros e agentes Bacillus thuringiensis Berliner on growth and survival of Noctuid de controle. Ribeirão Preto: USP/FFCLRP, 2001. 139p. (Dissertação (Lepidoptera) larvae. Journal of Economic Entomology, v.94, - Mestrado). p.752-759, 2001. NAP, J.P.; METS, P.L.J.; ESCALER, M.; CONNER, A.J. The release of WU, K.; GUO, Y.; LV, N.; GREENPLATE, J.T.; DEATON, R. Efficacy genetically modified crops into the environment. The Plant Journal, of transgenic cotton containing a cry1Ac gene from Bacillus v.33, p.1-18, 2003. thuringiensis against Helicoverpa armigera (Lepidoptera: Noctuidae) O’CALLAGHAN, M., GLARE, T.R.; BURGESS, E.P.J.; MALONE, in Northern China. Journal of Economic Entomology, v.96, p.1322- L.A. Effects of plants genetically modified for insect resistance on 1328, 2003. nontarget organisms. Annual Review of Entomology, v.50, p.271- ZWAHLEN, C.; NENTWIG, W.; BIGLER, F.; HILBECK, A. Tritrophic 292, 2005. interactions of transgenic Bacillus thuringiensis corn, Anaphothrips ORR, D.B.; LANDIS, D.A. Oviposition of European corn borer obscurus (Thysanoptera: Thripidae), and the predator Orius (Lepidoptera: Noctuidae) and impact of natural enemy population in majusculus (Heteroptera: Anthocoridae). Environmental transgenic versus isogenic corn. Journal of Economic Entomology, Entomology, v.9, p.846-850, 2000. v.90, p.805-809, 1997. PARON, M.J.F.O.; CRUZ, I.; CIOCIOLA, A.I. Efeito de genótipos de milho no parasitismo por Trichogramma spp. em ovos de Helicoverpa zea (Boddie). Anais da Sociedade Entomológica do Brasil, v.27, Received May 18, 2006 p.435-441, 1998. Accepted March 23, 2007

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