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Eficácia de milho transgênico tratado com inseticida no controle da lagarta-do-cartucho no milho safrinha no estado de São Paulo, Brasil

Efficacy of transgenic mayze insecticide treatment to control fall armyworm in late-season maize in São Paulo state, Brazil

RESUMO

Diversas tecnologias de milho geneticamente modificado (Bt) foram liberadas comercialmente desde 2007 visando principalmente o controle da lagarta-do-cartucho, Spodoptera frugiperda (Lepidoptera: Noctuidae). O objetivo deste trabalho foi avaliar a eficiência de híbridos transgênicos (Bt) e convencionais (não Bt) no controle lagarta-do-cartucho, submetidas ou não a inseticidas. Para isso, foram conduzidos ensaios em três localidades do estado de São Paulo nas safrinhas de 2009, 2010 e 2011, com delineamento experimental de blocos casualizados, em esquema fatorial 5x4, 5x4 e 8x4, respectivamente. O primeiro fator correspondeu ao número de híbridos comerciais de diferentes empresas. O segundo fator foi constituído pela utilização de diferentes manejos de controle do inseto. Para a avaliação dos danos ocasionados pela lagarta-do-cartucho, foram realizadas amostragens ao acaso de 20 plantas por parcela, aplicando-se uma escala de notas visuais, atribuindo notas que variam de 0 (sem dano) a 9 (cartucho totalmente destruído) e obtido a produtividade de grãos. Os dados foram submetidos à análise de variância e as médias comparadas pelo teste de Tukey a 5% de probabilidade, para cada parâmetro avaliado em cada localidade. Os híbridos transgênicos proporcionaram redução nas notas de danos atribuídas a lagarta-do-cartucho e as proteínas Cry 1F, Cry 1A105 e VIP3Aa20 foram as mais eficientes na redução do dano foliar. A pulverização mostrou-se uma estratégia eficiente em reduzir os danos foliar provocados pela praga. A combinação da pulverização com híbrido transgênico, de modo geral, mostrou ser uma boa estratégia para redução de dano foliar, especialmente quando foi utilizada a proteína Cry 1Ab, comprovadamente de menor eficiência para redução dos danos causados pela praga.

Termos para indexação:
Zea mays; Spodoptera frugiperda; manejo-de-pragas

ABSTRACT

Several genetically modified maize events expressing insecticidal proteins from Bacillus thuringiensis (Bt) have been commercially available in Brazil, intended to control of fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae). The objective of this study was to evaluate the efficiency of transgenic (Bt) and conventional (non-Bt) hybrids in the control of fall armyworm, treated or not with insecticides throughout three late growing seasons. To this end, trials were conducted at three locations in the state of São Paulo, in a randomized complete block design, in factorial arrangements with 5x4, 5x4 and 8x4 factors, respectively. The first factor consisted of the number of commercial hybrids of different companies. The second factor was represented by the different control managements of insect (non-Bt hybrid with and without insecticide; Bt hybrid with and without insecticide). The damage caused by fall armyworm was evaluated on a visual 1-9 scale, from score 0 (no damage) to 9 (totally destroyed whorl), and grain yield (kg ha-1). The data were analyzed by analysis of variance and the means compared by the Tukey test at 5% probability for each parameter evaluated at each location. For the Bt hybrids, the damage scores attributed to fall armyworm were lower and the proteins Cry 1F, Cry 1A105 and VIP3Aa20 were the most efficient in reducing leaf damage. Insecticide applications proved efficient in reducing leaf damage caused by the pest. Application of insecticides to Bt hybrids generally reduced leaf damage, especially for Cry1Ab-producing hybrids, which were the least effective in reducing pest damage without insecticides.

Index terms:
Zea mays; Spodoptera frugiperda; pest management

INTRODUCTION

Late-season maize in Brazil is characterized by rainfed cultivation, and is sown between January and April, after the summer crop, usually after early soybean. In the 2015 growing season, the acreage of late-season maize in the state of São Paulo was 370,100 hectares and the mean yield 4494 kg ha-1 (Conab, 2015COMPANHIA NACIONAL DE ABASTECIMENTO - CONAB. Acompanhamento da Safra Brasileira de Grãos, Safra 2013/2014, n.10. Brasília, DF: MAPA, 113p. Available in: <Available in: http://www.conab.gov.br/ >. Access in: December 10, 2015.
http://www.conab.gov.br/...
).

One of the main factors compromising the yield of late-season maize is the incidence of insect pests, whose populations have increased every year, reducing crop yields and thus causing losses to farmers (Fernandes; Carneiro, 2006FERNANDES, O. A.; CARNEIRO, T. R. Controle biológico de Spodoptera frugiperda no Brasil. In: PINTO, A. de S. et al. (Org.). Controle biológico de pragas na prática. Piracicaba: CP 2, 2006. p.75-82.).

One of the major pests is the fall armyworm, Spodoptera frugiperda (J.E. Smith, 1797) (Lepidoptera: Noctuidae) a polyphagous insect, which is widely distributed in tropical and subtropical regions of the Americas (Andrews, 1988ANDREWS, K. L. Latin American research on Spodoptera frugiperda (Lepidoptera: Noctuidae). Florida Entomologists, 71(4):630-653, 1988.), and is considered the main pest of maize in Brazil (Gallo et al., 2002GALLO, D. et al. Entomologia Agrícola. Piracicaba: FEALQ. 2002. 920p.; Cruz, 2008CRUZ, I. Manual de identificação de pragas do milho e de seus principais agentes de controle biológico. Brasília, DF: Embrapa Informação Tecnológica, 2008, 192p.).

As an alternative to control this pest, the use of transgenic (containing Bacillus thuringiensis - Bt) maize resistant to insects of the order Lepidoptera was admitted in Brazil. The first maize event was developed, characterized by expressing the insecticidal protein Cry 1AB, and was released on the market in Brazil in 2007. In the following year, another event expressing the insecticidal protein Cry 1F was launched (Carneiro et al., 2009CARNEIRO, A. A. et al. Milho Bt: Teoria e prática da produção de plantas transgênicas resistentes a insetos-praga. Sete Lagoas, MG: Embrapa Milho e Sorgo, 2009. 26p. (Circular Técnica, 135).; Storer et al., 2012STORER, N. P. et al. Status of resistance to Bt maize in Spodoptera frugiperda: Lessons from Puerto Rico. Journal of Invertebrate Pathology, 110(3):294-300, 2012.). Since then, other maize events with expression of different insecticidal proteins and even events with more than one protein were commercially released for the control of insects of the order Lepidoptera.

Prior to the development of Bt hybrids, the main control method was chemical, with synthetic insecticides, although the efficiency was rather variable. However even after the release of transgenic Bt maize hybrids in Brazil, insecticide applications were maintained, since initially, the suppression of S. frugiperda populations by Bt hybrids was merely partial.

Thus, the purpose of this study was to evaluate the effectiveness of these technologies in the control of S. frugiperda in three late growing seasons, in comparison with non-Bt isoline hybrids, sprayed or not with insecticides, in different regions of São Paulo state.

MATERIAL AND METHODS

The experiments were installed in March in the three regions Northwest of São Paulo, Central North and Mid Paranapanema during three late growing seasons (2009, 2010 and 2011). In the Northwest, the experiment was installed in Votuporanga, in the Central North in the city of Pindorama and in Mid Paranapanema, in the municipality of Maracaí in 2009 and 2011 and in Paraguaçu Paulista in 2010. In the experiments carried out in Pindorama the crops were irrigated.

In all experiments, a design with randomized blocks was used in a factorial arrangement of 5 x 4 (2009), 5 x 4 (2010) and 8 x 4 (2011), with four replications. The first factor corresponded to the number of commercial hybrids of different companies; these five were common to all growing seasons while in the last, three additional hybrids were tested. These hybrids were selected because at that time, they were marketed in a conventional and a transgenic version, in isolines with introgression of a gene derived from B. thuringiensis that confers resistance to lepidopteran pest species (Table 1).

Table 1:
Maize events, technology brands, toxins and non-Bt and Bt maize hybrids used in the experiments in the late growing seasons of 2009, 2010 and 2011.

The second factor consisted of different control managements of Lepidoptera: non-Bt hybrid without insecticide; non-Bt hybrid + insecticide; Bt hybrid without insecticide and Bt hybrid + insecticide. Per test, two to four insecticide sprayings (Table 2) were applied to maintain the plants at the lowest possible infestation level on a calendar. Insecticide sprayings of Bt and non-Bt hybrids were always applied at the same time.

Table 2:
Description of the experiments carried out in the late growing seasons of 2009, 2010 and 2011 at different locations in the state of São Paulo, Brazil.

The plots consisted of eight 10-m rows, and the evaluations were carried out in the four middle rows, discarding 1.5 m at either end of the row. The seeding density was between 55 and 57 thousand plants ha-1, for all hybrids in all experiments. The other cultural practices were applied according to the requirements of the no-tillage crop.

For the assessment of damage caused by fall armyworm, samples were randomly taken from 20 plants in the evaluated area of the plot, and assessed on a visual score scale, ranging from score 0 (no damage) to 9 (totally destroyed whorl), as proposed by Davis and Williams (1992DAVIS, F. M.; NG, S. S.; WILLIAMS, W. P. Visual rating scales for screening whorl-stage corn for resistance to fall armyworm. Mississippi: Agricultural and Forest Experiment Station, 1992. 9p. (Technical Bulletin, 186).), to assess the impact of leaf damage. These evaluations were carried out until flowering of plants began. To check the influence of S. frugiperda on the different tested hybrids and management types, analysis of variance was performed in the evaluation with highest scores of visual plant damage of each region.

To determine the yield (kg ha-1) of each treatment, harvest and threshing of maize ears were performed manually in two central rows of eight meters length and estimated by extrapolation of harvested production in 1 ha, with adjustment of the moisture content to 13%.

The data was analyzed by F test (ANOVA), at 5% probability and the means compared by the Tukey test at 5% probability, for meaning leaf damage score and grain yield at each location. All analyzes were carried using the ESTAT statistical software (Barbosa; Malheiros; Banzatto, 1992BARBOSA, J. C.; MALHEIROS, E. B.; BANZATTO, D. A. ESTAT: Um sistema de análises estatísticas de ensaios agronômicos. Jaboticabal: Unesp, 1992. Versão 2.0.).

RESULTS AND DISCUSSION

In the experiments of 2009, the damage caused by fall armyworm in the three regions was significant. However, in the Central North and Mid Paranapanema, the damage scores were initially low and tended to increase until the flowering of the plants, unlike in the Northwest, where the damage was high in the beginning and tended to decline thereafter (Figure 1).

Figure 1:
Symptom scores of visible damage (Davis Scale) of non-Bt and Bt maize hybrids with or without insecticide in three late growing seasons (2009, 2010 and 2011) in three regions of the state of São Paulo. The arrow indicates the evaluation used for analysis of variance.

In 2009, the differences between the factors hybrids and managements and the interaction between them in the three regions were significant for the scores of visual symptoms of S. frugiperda attack 35 days after emergence (DAE) in the Central North, 16 DAE in the Northwest and 39 DAE in the Mid Paranapanema region (Figure 1; Table 3).

Table 3:
Results of the F test for separate effects of maize hybrids and management types and of their interactions on the different parameters evaluated.

For the scores of S. frugiperda symptoms of unsprayed non-Bt hybrids, the most severely attacked hybrids were 30F35 in all three regions and 2B710 in the Central North and Mid Paranapanema, while hybrid DKB 350 was least attacked in the three regions (Table 4). Among the Bt hybrids, 30F35 Y with the YieldGard technology was the most attacked in the three regions, while the symptom scores of hybrid 2B710 HX (Herculex) were the lowest in all regions (Table 4), indicating differences in the efficiency of S. frugiperda control between the technologies YieldGard (Cry1Ab) and Herculex (Cry1F) in this season. It is noteworthy that these results were obtained in the years of early introduction of Bt maize, since the first transgenic maize seeds were sold in Brazil in 2008.

Table 4:
Partitioning of interactions for the visual symptoms of Spodoptera frugiperda between the hybrids and fall armyworm managements at four locations in the state of São Paulo.

According to the Seed Producers Association of São Paulo (APPS), the proportion of Bt maize seeds planted in the state of São Paulo was 52%, 69% and 73% in 2009, 2010 and 2011, respectively. Therefore, it is unlikely that the differences in results between the technologies were related to the development of genetic resistance by the pest.

In an experiment carried out in Georgia, United States, Buntin (2008BUNTIN, G. D. Corn expressing Cry1Ab or Cry1F endotoxin for fall armyworm and corn earworm (Lepidoptera: Noctuidae) management in field corn for grain production. Florida Entomologists , 91(4):523-530, 2008.) found that both events MON810 (Cry1Ab) and TC1507 (Cry1F) provided similar levels of protection against damage on the whorls of maize plants caused by S. frugiperda at low infestation levels and moderate infestation. However, at high infestation levels, hybrids with the insecticidal protein Cry1Ab were more attacked than those with Cry1F.

With regard to the management types, it was found that depending on the region, insecticide application significantly reduced the scores of S. frugiperda attack on non-Bt as well as Bt hybrids (Table 4). Insecticide application influenced the pest attack on Bt hybrids only in the Northwest region and specifically of hybrid 30F35Y. In the Mid Paranapanema and Central North, there were no differences between sprayed and unsprayed Bt hybrids due to the low armyworm infestation.

In the experiments of 2010, the intensity of S. frugiperda attack was higher than in the other years (Figure 1). In the Central North, there was a major S. frugiperda attack 49 DAE, in the Northwest 21 DAE, and in Mid Paranapanema, the attack rate was highest in the evaluation 56 DAE. In the case of the Northwest region, we decided to perform analysis of variance with plants 50 DAE for 21 DAE due to technical problems, since the treatments had not been sprayed with insecticide and therefore the damage caused by the larvae in these treatments was overestimated (Figure 1). For this parameter, significant differences were observed for the factors hybrids and managements separately and the interaction between both in all three regions, with exception of the Northwest region, where there was no significant difference within the factor hybrids (Table 3).

In the regions Mid Paranapanema and Central North, the lowest score attributed to S. frugiperda attack of unsprayed non-Bt hybrids was 6.53, however, no significant difference were observed between the scores of hybrids of this group (Table 5). In the Northwest region however, 30F35 was the most attacked (7.41) and DKB 350 the least attacked (3.89). Insecticide spraying caused a significant reduction in symptom scores in all regions and hybrids, except on 2B710 and Impacto in the Central North.

Table 5:
Partitioning of the effect of interactions between maize hybrids and management systems used on the scores ascribed to the symptoms of fall armyworm infestation on plants.

The scores attributed to Bt hybrids differed in all studied regions, indicating the control efficiency of the different technologies used in Brazil. The hybrids expressing the insecticidal protein Cry1Ab (DKB 350 YG and AG8088 YG) were the most attacked and hybrids expressing Cry1F (2B710 HX and 30F35 M) were significantly less attacked in all regions (Table 5).

Regarding the damage scores of sprayed transgenic hybrids, all Bt hybrids except those with the Herculex® technology, had lower scores when sprayed with insecticides, reinforcing the differences in efficiency of fall armyworm control between technologies the Yieldgard® and Agrisure TL (hybrids with insecticidal protein Cry1Ab) and Herculex® (with Cry1F) (Table 5). Although after insecticide spraying the damage scores of hybrids with protein Cry1Ab were similar to those with Cry1F technology, this type of management increases production costs (Table 5).

The fact that the hybrid expressing protein Cry1F is more effective in reducing S. frugiperda damage than hybrids expressing protein Cry1Ab was also reported by Siebert et al. (2008aSIEBERT, M. W. et al. Efficacy of Cry1F insecticidal protein in maize and cotton for control of fall armyworm (Lepidoptera: Noctuidae). Florida Entomologist, 91(4):555-565, 2008a., 2008bSIEBERT, M. W. et al. Evaluation of corn hybrids expressing Cry1F (Herculex I Insect Protection) against fall armyworm (Lepidoptera: Noctuidae) in the southern United States. Journal of Entomology Science, 43(1):41-51, 2008b.) and Hardke et al. (2011HARDKE, J. T. et al. Damage and survivorship o of fall armyworm (Lepidoptera: Noctuidae) on transgenic Field corn expressing Bacillus thuringiensis Cry proteins. Crop Protection, 30(2):168-172, 2011.).

In the 2011 late growing season, hybrids expressing new insecticidal proteins were released on the market (Table 2). In this growing season, only the Central North region continued under intensive fall armyworm attack (Figure 1).

Analysis of variance indicated significant differences in S. frugiperda infestation for the factors management and management x hybrid interaction in all three regions, but the factor hybrid was only significant in the Central North, where symptom scores were highest (Table 3). Partitioning the interaction indicated significant differences between non-Bt hybrids: in the Mid Paranapanema region the most attacked hybrid was Impacto (4.42) and the least Maximus (1.83) in the Northwest the most attacked was Maximus (5.51) and the least 30F35 (3.18) (Table 6).

Table 6:
Partitioning of the effect of interaction between the late season maize hybrids and fall armyworm managements on the scores for visual symptoms of pest attack.

With regard to the unsprayed Bt hybrids, the lowest levels of infestation were found in Maximus Viptera hybrids in all regions, and in AG8088 VTpro in the Mid Paranapanema and Central North regions. In the Central North, a highly infested region, the symptom scores of some Bt hybrids exceeded those of the non-Bt sprayed isolines, namely 30F35 Y, AG8088 YG and DKB 350 YG (Table 6). This fact indicates that the technology with Bt event YG was insufficient to protect plants from armyworm infestation.

This was the only region where spraying reduced the attack intensity on non-Bt hybrids, and specifically on the Bt hybrids expressing the insecticidal protein Cry1Ab (Table 6).

In relation to the variable grain yield, differences were significant in 2009 for the factors hybrids in the three regions, for managements in the Northwest and for hybrid x management interaction in the Central North and Northwest (Table 3).

The mean yield was highest in the Central North, mainly due to the use of irrigation. In this region, hybrid 30F35 was the most productive, regardless of the management (sprayed or unsprayed). Of the sprayed Bt hybrids, 30F35 Y was the most productive and DKB350 YG and Impacto TL were the least productive hybrids (Table 7).

Table 7:
Partitioning of interactions for grain yield (Kg ha-1) between late season maize hybrids and fall armyworm managements at two locations in the state of São Paulo.

Among conventional hybrids in the Northwest, hybrid AG8088 was also the highest-yielding, irrespective of the management (sprayed or unsprayed) and hybrid AG8088 YG (sprayed or unsprayed) was also the Bt hybrid with highest mean yield (Table 7).

For the management type in the Central North region, no significant differences were observed, while in the Northwest curiously the mean yield of unsprayed non-Bt hybrids was higher (6,065 kg ha-1), while the unsprayed Bt hybrids had lower mean yield (5,489 kg ha-1) (Table 7). In other words, the hybrid yield was not correlated with spraying, or with the tested pest control managements. The reason may have been that the scores indicated an insufficient level of leaf damage to cause a loss of grain yield.

In the late growing season of 2010, the differences for the factor hybrids were significant in all three regions, while for the factor managements and hybrid x management interaction, differences were only significant in the Mid Paranapanema region (Table 3).

Among the non-Bt hybrids without spraying, no significant differences were observed, however with spraying, hybrid 2B710 was the highest yielding (mean yield of 4.150 kg ha-1), and among the Bt hybrids (sprayed or unsprayed), Impacto TL, 2B710 HX, AG8088 YG and DKB350 YG were the most productive (Table 8).

Table 8:
Partitioning of the effect of interactions between maize hybrids and management systems on yield.

With regard to yield in Mid Paranapanema in the late season of 2011, the crop could not be harvested, due to frost damage. In the Central North, the differences between the factors hybrids and managements were significant, however there was no significant interaction between the two factors, since in the Northwest the factors hybrids and managements differed and there was a significant interaction between the factors as well (Table 3).

In the split analysis for the interaction between hybrids and managements, hybrid AG8088 was the most productive (5.343 kg ha-1) of the unsprayed non-Bt hybrids, and in response to spraying, the hybrids 2B710, AG8088 and Maximus were the most productive (approximately 4.942, 4.854 and 4.869 kg ha-1, respectively) (Table 9).

Table 9:
Partitioning of the effect of interactions between late season maize hybrids and fall armyworm managements on grain yield (kg ha-1) in Votuporanga, SP.

Regardless of the hybrids, to observe the adopted managements types, different from what occurred in 2009 and 2010, the combination of Bt hybrid plus spraying resulted in the highest mean yield (4,811 kg ha-1), while the management non-Bt hybrid + spraying induced the lowest mean yield (4,407 kg ha-1) (Table 9).

In field experiments, Lourenção and Fernandes (2013LOURENÇÃO, A. L. F.; FERNANDES, M. G. Avaliação do milho Bt Cry1Ab e Cry 1F no controle de Spodoptera frugiperda (J. E. Smith, 1797) (Lepidoptera: Noctuidae) em condições de campo. Científica, 41(2):164-188, 2013.) obtained results similar to those of this study, that the management of insecticide application plus use of Bt plants significantly reduced the damage caused by S. frugiperda. However, in relation to yield in the late growing seasons of 2009 and 2010, the results differ from those of Lourenção and Fernandes (2013)LOURENÇÃO, A. L. F.; FERNANDES, M. G. Avaliação do milho Bt Cry1Ab e Cry 1F no controle de Spodoptera frugiperda (J. E. Smith, 1797) (Lepidoptera: Noctuidae) em condições de campo. Científica, 41(2):164-188, 2013.. In the late growing season of 2010, in experiments in Mato Grosso do Sul, these authors found that the combination of Bt hybrid with insecticide spraying induced the highest yields, exceeding those obtained in other tested management types.

This fact was observed by Gurian-Sherman (2009)GURIAN-SHERMAN, D. Failure to Yield: Evaluating the performance of genetically modified crops. The Union of Concerned Scientists (UCS). 2009. 51p. Available in: <Available in: http://www.ucsusa.org/assets/documents/food_and_agriculture/failure-to-yield.pdf >. Access in: October 10, 2014.
http://www.ucsusa.org/assets/documents/f...
, who reported that the yield gains in Bt plants are not significant when compared to conventional plants. In studies the United States, these authors also estimated that Bt maize resistant to Ostrinia nubilalis produced a 7.0 to 12% higher yield than non-Bt lines during periods of high infestation, but offers little or no advantage when infestation is low or moderate.

CONCLUSIONS

Transgenic hybrids reduced the damage scores attributed to fall armyworm and those expressing the proteins Cry1F, Cry1A105, and VIP3Aa20 were the most efficient in reducing leaf damage. Spraying was an effective strategy in reducing leaf damage caused by the pest. In general, the combination of spraying with a Bt hybrid, proved a good strategy to reduce leaf damage, especially when using protein Cry 1ab, which is known to be less efficient in reducing the damage caused by the pest.

ACKNOWLEDGEMENT

The authors thank Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Proc. No. 2010/02666-8) for their financial support.

REFERENCES

  • ANDREWS, K. L. Latin American research on Spodoptera frugiperda (Lepidoptera: Noctuidae). Florida Entomologists, 71(4):630-653, 1988.
  • BARBOSA, J. C.; MALHEIROS, E. B.; BANZATTO, D. A. ESTAT: Um sistema de análises estatísticas de ensaios agronômicos. Jaboticabal: Unesp, 1992. Versão 2.0.
  • BUNTIN, G. D. Corn expressing Cry1Ab or Cry1F endotoxin for fall armyworm and corn earworm (Lepidoptera: Noctuidae) management in field corn for grain production. Florida Entomologists , 91(4):523-530, 2008.
  • CARNEIRO, A. A. et al. Milho Bt: Teoria e prática da produção de plantas transgênicas resistentes a insetos-praga. Sete Lagoas, MG: Embrapa Milho e Sorgo, 2009. 26p. (Circular Técnica, 135).
  • COMPANHIA NACIONAL DE ABASTECIMENTO - CONAB. Acompanhamento da Safra Brasileira de Grãos, Safra 2013/2014, n.10. Brasília, DF: MAPA, 113p. Available in: <Available in: http://www.conab.gov.br/ >. Access in: December 10, 2015.
    » http://www.conab.gov.br/
  • CRUZ, I. Manual de identificação de pragas do milho e de seus principais agentes de controle biológico. Brasília, DF: Embrapa Informação Tecnológica, 2008, 192p.
  • DAVIS, F. M.; NG, S. S.; WILLIAMS, W. P. Visual rating scales for screening whorl-stage corn for resistance to fall armyworm. Mississippi: Agricultural and Forest Experiment Station, 1992. 9p. (Technical Bulletin, 186).
  • FERNANDES, O. A.; CARNEIRO, T. R. Controle biológico de Spodoptera frugiperda no Brasil. In: PINTO, A. de S. et al. (Org.). Controle biológico de pragas na prática. Piracicaba: CP 2, 2006. p.75-82.
  • GALLO, D. et al. Entomologia Agrícola. Piracicaba: FEALQ. 2002. 920p.
  • GURIAN-SHERMAN, D. Failure to Yield: Evaluating the performance of genetically modified crops. The Union of Concerned Scientists (UCS). 2009. 51p. Available in: <Available in: http://www.ucsusa.org/assets/documents/food_and_agriculture/failure-to-yield.pdf >. Access in: October 10, 2014.
    » http://www.ucsusa.org/assets/documents/food_and_agriculture/failure-to-yield.pdf
  • HARDKE, J. T. et al. Damage and survivorship o of fall armyworm (Lepidoptera: Noctuidae) on transgenic Field corn expressing Bacillus thuringiensis Cry proteins. Crop Protection, 30(2):168-172, 2011.
  • LOURENÇÃO, A. L. F.; FERNANDES, M. G. Avaliação do milho Bt Cry1Ab e Cry 1F no controle de Spodoptera frugiperda (J. E. Smith, 1797) (Lepidoptera: Noctuidae) em condições de campo. Científica, 41(2):164-188, 2013.
  • SIEBERT, M. W. et al. Efficacy of Cry1F insecticidal protein in maize and cotton for control of fall armyworm (Lepidoptera: Noctuidae). Florida Entomologist, 91(4):555-565, 2008a.
  • SIEBERT, M. W. et al. Evaluation of corn hybrids expressing Cry1F (Herculex I Insect Protection) against fall armyworm (Lepidoptera: Noctuidae) in the southern United States. Journal of Entomology Science, 43(1):41-51, 2008b.
  • STORER, N. P. et al. Status of resistance to Bt maize in Spodoptera frugiperda: Lessons from Puerto Rico. Journal of Invertebrate Pathology, 110(3):294-300, 2012.

Datas de Publicação

  • Publicação nesta coleção
    Mar-Apr 2017

Histórico

  • Recebido
    17 Maio 2016
  • Aceito
    05 Dez 2016
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