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Fall armyworm (FAW), Spodoptera frugiperda (Smith), is one of the major pests targeted by transgenic crops expressing insecticidal proteins from Bacillus thuringiensis (Bt) Berliner. However, FAW presents a high capacity to develop resistance to Bt protein-expressing crop lines, as reported in Brazil, Argentina, Puerto Rico and the southeastern U.S. Here, FAW genotypes resistant to pyramided maize events expressing Cry1F/Cry1A.105/Cry2Ab2 (P-R genotype) and Cry1A.105/Cry2Ab2 (Y-R genotype) from Brazil were used to investigate the interactions between non-Bt hosts (non-Bt maize, non-Bt cotton, millet and sorghum) and fitness costs. We also tested a FAW genotype susceptible to Bt maize and F1 hybrids of the resistant and susceptible genotypes (heterozygotes). Recessive fitness costs (i.e., costs affecting the resistant insects) were observed for pupal and neonate to adult survival of the P-R genotype on non-Bt cotton; larval developmental time of the P-R genotype on millet and sorghum; larval and neonate-to-adult developmental time of the Y-R genotype on non-Bt cotton and sorghum; the fecundity of the Y-R genotype on non-Bt cotton; and mean generation time of both resistant genotypes. However, on non-Bt cotton and non-Bt maize, the P-R genotype had a higher fitness (i.e., fitness benefits), displaying greater fecundity and rates of population increases than the Sus genotype. Non-recessive fitness costs (i.e., costs affecting heterozygotes) were found for fecundity and population increases on millet and sorghum. These findings suggest that, regardless of the disadvantages of the resistant genotypes in some hosts, the resistance of FAW to Cry1 and Cry2 Bt proteins is not linked with substantial fitness costs, and may persist in field conditions once present.

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BACKGROUND: The use of Bt plants has been the main strategy for controlling the fall armyworm Spodoptera frugiperda (J. E. Smith) in Brazil. However, many resistance cases were already registered. The resistance of S. frugiperda to the Vip3Aa20 protein was recently characterized under laboratory conditions but it is still efficient under field conditions. Here, resistance monitoring studies were conducted using phenotypic (purified protein and Bt maize leaves) and genotypic (F1 and F2 screen) methods to support insect resistance management (IRM) programs and preserve Vip3Aa20 technology on maize. RESULTS: Phenotypic monitoring with purified protein showed two populations significantly different from the susceptible strain on the second crop season in 2016. This number increased for the first and second crop seasons in 2017 in several regions. The genotypic monitoring estimated a mean frequency of the resistance allele of 0.0027 for the F1 screen and 0.0033 for the F2 screen. Three new resistant strains to Vip3Aa20 were selected from F2 screen assays. Complementation tests on these new resistant strains were positive with the previous resistant strain. CONCLUSION: Here we showed that the resistance allele of S. frugiperda to Vip3Aa20 protein is widely distributed in maize-producing regions in Brazil and its frequency increases throughout crop seasons. © 2019 Society of Chemical Industry.

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The biphasic dose-response of a stressor where low amounts of a toxicant may stimulate some biological processes is a recent focus of attention in insecticide ecotoxicology. Nonetheless, the importance and management consequences of this phenomenon of pesticide-induced hormesis remain largely unrecognized. Curiously, the potential induction of hormesis by insecticidal proteins such as Bacillus thuringiensis toxins (i.e., Bt toxins), a major agriculture pest management tool of widespread use, has been wholly neglected. Thus, we aimed to circumvent this shortcoming while assessing the potential occurrence of hormesis induced by the Bt toxin Cry1Fa in its main target pest species - the fall armyworm Spodoptera frugiperda. Concentration-response bioassays were carried out in a Bt-susceptible and a Bt-resistant population providing the purified Cry1Fa toxin in artificial diet and recording the insect demographic parameters. As significant hormetic effect was detected in both populations with a significant increase in the net reproductive rate and the intrinsic rate of population growth, the potential occurrence of Bt-induced hormesis was subsequently tested providing the insects with leaves from transgenic Bt maize expressing the toxic protein. The performance of the Bt-resistant insects was not different in both maize genotypes, indicating that the leaf expression of the Bt protein did not promote hormesis in the resistant insects. Thus, despite the Bt-induced hormesis detected in the purified protein bioassays, the phenomenon was not detected with current levels of Bt expression in maize minimizing the risk of this additional efficacy constraint besides that of field occurrence of Bt resistance.

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Field studies across four states in maize-producing areas of Brazil were conducted to characterize the efficacy of a new pyramided Bacillus thuringiensis (Bt) Berliner technology in maize, Zea mays L., and compare it to existing single and pyramided commercial Bt technologies, to control Helicoverpa zea Boddie (Lepidoptera: Noctuidae), Elasmopalpus lignosellus Zeller (Lepidoptera: Pyralidae), Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae), and Diatraea saccharalis F. (Lepidoptera: Crambidae). Bt maize expressing Vip3Aa20 protein and pyramided Bt maize expressing proteins Cry1F + Cry1A.105 + Cry2Ab2 + Vip3Aa20 provided excellent protection against kernel feeding by H. zea compared to Bt technologies expressing only Cry1F or Cry1A.105 + Cry2Ab2. Bt maize expressing Cry1F, Cry1A.105 + Cry2Ab2, Cry1F + Cry1A.105 + Cry2Ab2, and Cry1F + Cry1A.105 + Cry2Ab2 + Vip3Aa20 resulted in less than 5% of plants injured by E. lignosellus, significantly less than Bt maize expressing only Vip3Aa20 and a non-Bt maize iso-hybrid with and without a thiamethoxam seed treatment. The highest protection against plant cutting injury caused by A. ipsilon was observed in the pyramid Bt maize technology expressing Cry1F + Cry1A.105 + Cry2Ab2 + Vip3Aa20. However, it did not differ statistically from the Bt maize expressing Vip3Aa20, Cry1F, or Cry1F + Cry1A.105 + Cry2Ab2. All Bt maize hybrids evaluated in our study were highly effective in reducing tunneling injury caused by D. saccharalis. These results show that a new maize technology expressing pyramided Bt proteins Cry1F + Cry1A.105 + Cry2Ab2 + Vip3Aa20 offers a higher level of protection from feeding by the above lepidopteran pest complex compared to maize with a single Bt protein or double pyramided Bt proteins.

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The resistance of fall armyworm, Spodoptera frugiperda, has been characterized to Cry and Vip3A proteins of Bacillus thuringiensis (Bt) expressed in maize in Brazil. Here, we investigate the cross-resistance to Bt-insecticide XenTari in selected fall armyworm strains resistant to Bt maize varieties. The LC50 of XenTari in neonates of resistant strains ranged from 0.28 to 0.68 µg a.i./cm2, while for the susceptible reference strain (Sus), LC50 was 0.21 µg a.i./cm2. This indicated a resistance ratio lower than 3.2-fold. A similar variation in susceptibility was detected in EC50 values, which ranged from 0.04 to 0.13 µg a.i./cm2, demonstrating a maximum resistance ratio of 4.3-fold relative to the Sus strain (EC50 = 0.03 µg a.i./cm2). In the F1 progeny from reciprocal crosses, the LC50 ranged from 0.28 to 0.64 µg a.i./cm2 and EC50 from 0.03 to 0.18 µg a.i./cm2, similar to the values verified in parental resistant strains and representing a maximum resistance ratio of 3.0 and 6.0-fold, respectively. We also determined that susceptibility of third instar larvae to XenTari decreased when compared to neonates, however the variation remained similar. For third instar larvae from resistant strains, LC50 of XenTari ranged from 10.79 to 39.85 µg a.i./cm2, while for the Sus strain, LC50 was 9.25 µg a.i./cm2 (resistance ratio inferior to 4.3-fold). At the same stage, in heterozygous strains the LC50 ranged from 14.75 to 58.47 µg a.i./cm2 (resistance ratio inferior to 6.3-fold). Our data demonstrate a lack of significant cross-resistance to Bt-based insecticide XenTari in fall armyworm strains with resistance to Bt maize varieties.

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Evolution of resistance to control measures in insect populations is a natural process, and management practices are intended to delay or mitigate resistance when it occurs. During the 2012/13 season the first reports of unexpected damage by Diatraea saccharalis on some Bt maize hybrids occurred in the northeast of San Luis province, Argentina. The affected Bt technologies were Herculex I® (HX-TC1507) and VT3PRO® (MON 89034 × MON 88017*). Event TC1507 expresses Cry1F and event MON 89034 expresses Cry1A.105 and Cry2Ab2, whichr are all Bt proteins with activity against the lepidopterans D. saccharalis and Spodoptera frugiperda (MON 88017 expresses the protein Cry3Bb1 for control of coleopteran insects and the enzyme CP4EPSPS for glyphosate tolerance). The affected area is an isolated region surrounded by sierra systems to the northeast and west, with a hot semi-arid climate, long frost-free period, warm winters, hot dry summers, and woody shrubs as native flora. To manage and mitigate the development of resistance, joint actions were taken by the industry, growers and Governmental Agencies. Hybrids expressing Vip3A protein (event MIR162) and/or Cry1Ab protein (events MON 810 and Bt11) as single or stacked events are used in early plantings to control the first generations of D. saccharalis, and in later plantings date's technologies with good control of S. frugiperda. A commitment was made to plant the refuge, and pest damage is monitored. As a result, maize production in the area is sustainable and profitable with yields above the average.

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Transgenic maize expressing the insecticidal protein Vip3Aa20 is increasingly being adopted in Brazil. In this study, we determined the baseline susceptibility of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) and Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) to Vip3Aa20, as part of an Insect Resistance Management (IRM) program. Diet-overlay bioassays were conducted with neonates exposed to Vip3Aa20 for 7 d. The baseline susceptibility data were obtained for seven field populations of H. armigera and six of H. zea collected from major soybean-, cotton-, and maize-producing areas in Brazil. To validate the diagnostic concentration, 11 field populations of H. zea were tested from 2014 to 2015. The LC50 for H. armigera populations ranged from 2.97 to 8.41 µg Vip3Aa20/cm2 (threefold variation), and for H. zea populations from 0.04 to 0.21 µg Vip3Aa20/cm2 (fivefold variation). The EC50 for H. armigera ranged from 0.099 to 0.455 µg Vip3Aa20/cm2 (fivefold variation), and for H. zea from 0.004 to 0.020 µg Vip3Aa20/cm2 (fivefold variation). H. armigera was more tolerant to Vip3Aa20 protein than was H. zea (≈40- to 75-fold, based on LC50). Based on the LC99 value, the concentration of 6.4 µg Vip3Aa20/cm2 was defined as a diagnostic concentration for susceptibility monitoring in H. zea, and >44 µg Vip3Aa20/cm2 for H. armigera. Our baseline susceptibility data for Vip3Aa20 in H. armigera and H. zea populations will be useful in IRM programs in Brazil.

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BACKGROUND: The frequency of resistance alleles is a major factor influencing the rate of resistance evolution. Here, we adapted the F2 screen procedure for Spodoptera frugiperda (J. E. Smith) with a discriminating concentration assay, and extended associated statistical methods to estimate the frequency of resistance to Cry1F protein in S. frugiperda in Brazil when resistance was not rare. RESULTS: We show that F2 screen is efficient even when the resistance frequency is 0.250. It was possible to screen 517 isoparental lines from 12 populations sampled in five states of Brazil during the first half of 2012. Western Bahia had the highest allele frequency of Cry1F resistance, 0.192, with a 95% confidence interval (CI) between 0.163 and 0.220. All other states had a similar and lower frequency varying from 0.042 in Paraná to 0.080 in Mato Grosso do Sul. CONCLUSION: The high frequency in western Bahia may be related to year-round availability of maize, the high population density of S. frugiperda, the lack of refuges and the high adoption rate of Cry1F maize. Cry1F resistance alleles were not rare and occurred at frequencies that have already compromised the useful life of TC1507 maize in western Bahia. © 2016 Society of Chemical Industry.

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BACKGROUND: Spodoptera frugiperda is one the main target pests of maize events expressing Vip3Aa20 protein from Bacillus thuringiensis (Bt) in Brazil. In this study, we selected a resistant strain of S. frugiperda on Bt maize expressing Vip3Aa20 protein and characterized the inheritance and fitness costs of the resistance. RESULTS: The resistance ratio of the Vip3Aa20-resistant strain of S. frugiperda was >3200-fold. Neonates of the Vip3Aa20-resistant strain were able to survive and emerge as fertile adults on Vip3Aa20 maize, while larvae from susceptible and heterozygous strains did not survive. The inheritance of Vip3Aa20 resistance was autosomal recessive and monogenic. Life history studies to investigate fitness cost revealed an 11% reduction in the survival rate until adult stage and a ∼50% lower reproductive rate of the Vip3Aa20-resistant strain compared with susceptible and heterozygous strains. CONCLUSION: This is the first characterization of S. frugiperda resistance to Vip3Aa protein. Our results provide useful information for resistance management programs designed to prevent or delay resistance evolution to Vip3Aa proteins in S. frugiperda. © 2016 Society of Chemical Industry.

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BACKGROUND: The first Bt maize in Brazil was launched in 2008 and contained the MON 810 event, which expresses Cry1Ab protein. Although the Cry1Ab dose in MON 810 is not high against fall armyworm (FAW), Spodoptera frugiperda (J.E. Smith), MON 810 provided commercial levels of control. To support insect resistance management in Brazil, the baseline and ongoing susceptibility of FAW was examined using protein bioassays, and the level of control and life history parameters of FAW were evaluated on MON 810 maize. RESULTS: Baseline diet overlay assays with Cry1Ab (16 µg cm(-2) ) caused 76.3% mortality to field FAW populations sampled in 2009. Moderate mortality (48.8%) and significant growth inhibition (88.4%) were verified in leaf-disc bioassays. In greenhouse trials, MON 810 had significantly less damage than non-Bt maize. The surviving FAW larvae on MON 810 (22.4%) had a 5.5 day increase in life cycle time and a 24% reduction in population growth rate. Resistance monitoring (2010-2015) showed a significant reduction in Cry1Ab susceptibility of FAW over time. Additionally, a significant reduction in the field efficacy of MON 810 maize against FAW was observed in different regions from crop season 2009 to 2013. CONCLUSIONS: The decrease in susceptibility to Cry1Ab was expected, but the specific contributions to this resistance by MON 810 maize cannot be distinguished from cross-resistance to Cry1Ab caused by exposure to Cry1F maize. Technologies combining multiple novel insecticidal traits with no cross-resistance to the current Cry1 proteins and high activity against the same target pests should be pursued in Brazil and similar environments. © 2015 Society of Chemical Industry.

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