Fall armyworm (Lepidoptera: Noctuidae): practical resistance of 2 Brazilian populations to Cry1A.105†+†Cry2Ab and Cry1F Bt maize.

In the Americas, transgenic crops producing insecticidal proteins from Bacillus thuringiensis Berliner (Bt, Bacillales: Bacillaceae) have been used widely to manage fall armyworm (FAW, Spodoptera frugiperda [J.E. Smith]). As resistance to Cry1 single-gene Bt maize (Zea mays L.) rapidly evolved in some FAW populations, pyramided Bt maize hybrids producing Cry1, Cry2, or Vip3Aa proteins were introduced in the 2010s. We examined field-evolved resistance to single- and dual-protein Bt maize hybrids in 2 locations in southeastern Brazil, where plant damage by FAW larvae far exceeded the economic threshold in 2017. We collected late-instar larvae in Cry1A.105 + Cry2Ab and Cry1F maize fields and established 2 FAW populations in the laboratory. The F1 offspring reared on the foliage of Bt and non-Bt maize plants (Cry1A.105 + Cry2Ab and Cry1F) showed neonate-to-adult survival rates as high as 70% for both populations. There was no significant difference in the life-table parameters of armyworms reared on non-Bt and Bt maize foliage, indicating complete resistance to Cry1A.105 + Cry2Ab maize. Larval survival rates of reciprocal crosses of a susceptible laboratory strain and the field-collected populations indicated nonrecessive resistance to Cry1F and a recessive resistance to Cry1A.105 + Cry2Ab maize. When relaxing the selection pressure, the armyworm fitness varied on Cry1A.105 + Cry2Ab and non-Bt maize; the resistance was somewhat stable across 12 generations, without strong fitness costs, although one of the lines died confounded by a depleted-quality, artificial rearing diet. To our knowledge, this is the first report documenting the practical resistance of FAW to a pyramided Bt crop. We discuss the implications for resistance management.

Plant Resistance in Some Modern Soybean Varieties May Favor Population Growth and Modify the Stylet Penetration of Bemisia tabaci (Hemiptera: Aleyrodidae).

Complaints of severe damage by whiteflies in soybean fields containing genetically engineered (GE) varieties led us to investigate the role of transgenic soybean varieties expressing resistance to some insects (Cry1Ac Bt toxin) and to herbicide (glyphosate) on the population growth and feeding behavior of Bemisia tabaci (Gennadius) MEAM1 (Hemiptera: Aleyrodidae). In the laboratory, the whiteflies reared on the GE Bt soybeans had a net reproductive rate (R0) 100% higher and intrinsic rate of population increase (rm) 15% higher than those reared on non-GE soybeans. The increased demographic performance was associated with a higher lifetime fecundity. In electrical penetration graphs, the whiteflies reared on the GE soybeans had fewer probes and spent 50% less time before reaching the phloem phase from the beginning of the first successful probe, indicating a higher risk of transmission of whitefly-borne viruses. Data from Neotropical fields showed a higher population density of B. tabaci on two soybean varieties expressing glyphosate resistance and Cry1Ac Bt toxin. These results indicate that some GE soybean varieties expressing insect and herbicide resistances can be more susceptible to whiteflies than non-GE ones or those only expressing herbicide resistance. Most likely, these differences are related to varietal features that increase host-plant susceptibility to whiteflies. Appropriate pest management may be needed to deal with whiteflies in soybean fields, especially in warm regions, and breeders may want to consider the issue when developing new soybean varieties.

Demographic Performance of Helicoverpa zea Populations on Dual and Triple-Gene Bt Cotton.

Insecticidal toxins from Bacillus thuringiensis (Bt) are valuable tools for pest management worldwide, contributing to the management of human disease insect vectors and phytophagous insect pests of agriculture and forestry. Here, we report the effects of dual and triple Bt toxins expressed in transgenic cotton cultivars on the fitness and demographic performance of Helicoverpa zea (Boddie)-a noctuid pest, known as cotton bollworm and corn earworm. Life-history traits were determined for individuals of three field populations from a region where H. zea overwintering is likely. Triple-gene Bt cotton cultivars that express Cry and Vip3Aa toxins killed 100% of the larvae in all populations tested. In contrast, dual-gene Bt cotton that express Cry1Ac+Cry1F and Cry1Ac+Cry2Ab allowed population growth with the intrinsic rate of population growth (rm) 38% lower than on non-Bt cotton. The insects feeding on Bt cotton plants that express Cry1Ac+Cry2Ab, Cry1Ac+Cry1F, or Cry1Ab+Cry2Ae exhibited reduced larval weight, survival rate, and increased development time. Additionally, fitness parameters varied significantly among the insect populations, even on non-Bt cotton plants, likely because of their different genetic background and/or previous Bt toxin exposure. This is the first report of the comparative fitness of H. zea field populations on dual-gene Bt cotton after the recent reports of field resistance to certain Bt toxins. These results document the population growth rates of H. zea from an agricultural landscape with 100% Bt cotton cultivars. Our results will contribute to the development and validation of resistance management recommendations.

Contrasting susceptibility of lepidopteran pests to diamide and pyrethroid insecticides in a region of overwintering and migratory intersection.

BACKGROUND: Pesticide resistance is a growing issue worldwide, and susceptibility of pest populations should be monitored in migratory intersection regions for successful resistance management. We determined the susceptibility of eight noctuid species from the Florida Panhandle to bifenthrin (pyrethroid) and chlorantraniliprole (diamide). Larvae from field and laboratory populations were exposed to commercial insecticide formulations using the leaf-dip method in concentration-mortality bioassays. RESULTS: The field populations of Helicoverpa zea (Boddie), Spodoptera frugiperda (Smith), S. eridania (Stoll), S. exigua (Hubner) and Chloridea virescens (Fabricius) had reduced susceptibility to bifenthrin compared with the laboratory populations. Resistance ratios to bifenthrin were as high as 10 071-fold in S. exigua and 436-fold in S. frugiperda, while there was no reduced susceptibility in Agrotis ipsilon (Hufnagel). The susceptibility to chlorantraniliprole was similar between the field and laboratory populations studied, except for S. exigua that exhibited 630-fold resistance to the diamide. The probit regression equations indicated that the larval mortality of S. exigua and S. frugiperda populations was <80% with bifenthrin at the concentration equivalent to the label rate. Likewise, the estimated mortality of S. exigua larvae with chlorantraniliprole at the label rate concentration was <80%. CONCLUSIONS: The lepidopteran pest populations tested were variable in susceptibility to bifenthrin by contrast to more consistent susceptibility to chlorantraniliprole. These results help in the choice of effective insecticides for integrated pest management and resistance management in cropping systems colonized by migratory lepidopteran pests from the U.S. Gulf Coast region. © 2020 Society of Chemical Industry.

Like Parents, Like Offspring? Susceptibility to Bt Toxins, Development on Dual-Gene Bt Cotton, and Parental Effect of Cry1Ac on a Nontarget Lepidopteran Pest.

An important step to devise appropriate pest management strategies for armyworms (Lepidoptera: Noctuidae) in Bacillus thuringiensis Berliner (Bt) crops is to determine the lethal, sublethal, and parental effects of Bt toxins on target and nontarget pest species. Here we documented the susceptibility of black armyworm, Spodoptera cosmioides (Walker), to three Cry toxins and its life-history traits feeding on dual-toxin Bt cotton and an artificial diet containing sublethal concentrations of Cry1Ac. In concentration-response bioassays, black armyworm larvae showed low susceptibility to Cry toxins, with 853 ng/cm2 as the lowest value estimated for the median lethal concentration (LC50). The decreasing rank of toxicity was Cry1F, Cry2Aa, and Cry1Ac. Foliage of dual-toxin Bt cotton varieties (Cry1Ac + Cry1F and Cry1Ab + Cry2Ae) caused higher larval mortality than Cry1Ac-expressing cotton. Black armyworms showed reduced larval weight when growing on the Cry1Ac-treated diet, yet they reached adulthood and produced offspring. Interestingly, these larvae were grown on the control diet and showed reduced weight gain associated with the toxin exposure of the previous generation, indicating a parental effect of the exposure to Cy1Ac. The reduced larval weight was recovered in later instars, and there was no significant change in the population fitness of the parental armyworms or their offspring. To our knowledge, this is the first study documenting the parental effects of Bt toxins in insects. These results advance our understanding of potential responses of nontarget species when exposed to Bt toxins and contribute to design pest management programs for armyworms and other nontarget lepidopteran species exposed to Bt crops.

Bt-induced hormesis in Bt-resistant insects: Theoretical possibility or factual concern?

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.

Yield Losses in Transgenic Cry1Ab and Non-Bt Corn as Assessed Using a Crop-Life-Table Approach.

In this study, we constructed crop life tables for Bacillus thuringiensis Berliner (Bt) Cry1Ab and non-Bt corn hybrids, in which yield-loss factors and abundance of predaceous arthropods were recorded during 2 yr at two locations. Corn kernel/grain was the yield component that had the heaviest losses and that determined the overall yield loss in the corn hybrids across years and locations. Yield losses in both corn hybrids were primarily caused by kernel-destroying insects. Helicoverpa zea (Boddie) and Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae) were the key loss factors at one location, while at the other, the key loss factor was the silk fly larvae, Euxesta spp. (Diptera: Ulidiidae). Although the realized yield of corn grains was not different (P > 0.05) between Cry1Ab and non-Bt corn hybrids, the Bt corn hybrid reduced (P < 0.05) the damage by H. zea and S. frugiperda in three of the four field trials, particularly at the location where Lepidoptera were the key loss factors. As expected, no reduction in the abundance of predaceous arthropods was observed in Cry1Ab corn fields. Various species of natural enemies were recorded, particularly the earwig Doru luteipes (Scudder) (Dermaptera: Forficulidae), which was the most abundant and frequent predaceous insect. These results indicate that integration of pest management practices should be pursued to effectively minimize losses by kernel-destroying insects during corn reproductive stages when growing non-Bt or certain low-dose Bt corn cultivars for fall armyworm and corn earworm, such as those producing Cry1Ab or other Cry toxins.

Host-Plant Resistance to Spittlebugs: A Life-Table Study With Mahanarva fimbriolata (Hemipera: Cercopidae) in Sugarcane Genotypes.

Understanding how host-crop genotypes affect the life history of insect pests is important for developing and using varietal resistance as a pest control measure. Here we determined how wild and cultivated sugarcane genotypes affect key life-history traits and the demographic performance of the root spittlebug, Mahanarva fimbriolata (Stål; Hemiptera: Cercopidae), a major pest of sugarcane, which produces most of the world's sugar and bioethanol. In the greenhouse, plants of four sugarcane genotypes (two wild and two cultivated) were infested with newly-ecloded spittlebug nymphs. A longitudinal life-table experiment was conducted recording developmental time, survival, reproductive output, and longevity of the released spittlebug nymphs. One of the promising sugarcane genotypes was the accession IM76-229 (Saccharum robustum Brandes & Jesw. ex Grassl), which allowed only 20% of nymph survival to adulthood and reduced the spittlebug longevity by 10 d. Such effects on these life-history traits led to a negative intrinsic rate of population growth (rm = -0.002) of the insects, indicating that the test population would eventually go extinct on this sugarcane genotype. An opposite trend (i.e., population growth) was obtained for the insects raised on Saccharum spp. (SP81-3250 and SP80-1816 cultivars) and Erianthus arundinaceus (Retz) Jeswiet (Kawandang genotype). These results show that S. robustum IM76-229 genotype has resistance traits that drastically reduce spittlebug population growth and indicate that it can be used in breeding programs aiming to develop sugarcane cultivars with resistance to spittlebugs.

Fitness costs and stability of Cry1Fa resistance in Brazilian populations of Spodoptera frugiperda.

BACKGROUND: The presence of fitness costs of resistance to Bacillus thuringiensis (Bt) insecticidal proteins in insect populations may delay or even reverse the local selection of insect resistance to Bt transgenic crops, and deserves rigorous investigation. Here we assessed the fitness costs associated with Cry1Fa resistance in two strains of fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), derived from field collections in different Brazilian regions and further selected in the laboratory for high levels of resistance to Cry1Fa using leaves of TC1507 corn. RESULTS: Fitness components were compared using paired resistant and susceptible strains with similar genetic backgrounds and F1 generations from reciprocal crosses, all of them reared on non-transgenic corn leaves. No apparent life history costs in the larval stage were observed in the Bt-resistant strains. Moreover, the resistance remained stable for seven generations in the absence of selection, with no decrease in the proportion of resistant individuals. Larval respiration rates were also similar between resistant and susceptible homozygotes, and heterozygotes displayed respiration rates and demographic performance equal or superior to those of susceptible homozygotes. CONCLUSION: In combination, these results indicate the lack of strong fitness costs associated with resistance to Cry1Fa in the fall armyworm strains studied. These findings suggest that Cry1Fa resistance in S. frugiperda populations is unlikely to be counterselected in Cry1Fa-free environments. © 2016 Society of Chemical Industry.

Locomotory and physiological responses induced by clove and cinnamon essential oils in the maize weevil Sitophilus zeamais.

Plant essential oils have been suggested as a suitable alternative for controlling stored pests worldwide. However, very little is known about the physiological or behavioral responses induced by these compounds in insect populations that are resistant to traditional insecticides. Thus, this investigation evaluated the toxicity (including the impacts on population growth) as well as the locomotory and respiratory responses induced by clove, Syzygium aromaticum L., and cinnamon, Cinnamomum zeylanicum L., essential oils in Brazilian populations of the maize weevil Sitophilus zeamais. We used populations that are resistant to phosphine and pyrethroids (PyPhR), only resistant to pyrethroids (PyR1 and PyR2) or susceptible to both insecticide types (SUS). The PyPhR population was more tolerant to cinnamon essential oil, and its population growth rate was less affected by both oil types. Insects from this population reduced their respiratory rates (i.e., CO2 production) after being exposed to both oil types and avoided (in free choice-experiments) or reduced their mobility on essential oil-treated surfaces. The PyR1 and PyR2 populations reduced their respiratory rates, avoided (without changing their locomotory behavior in no-choice experiments) essential oil-treated surfaces and their population growth rates were severely affected by both oil types. Individuals from SUS population increased their mobility on surfaces that were treated with both oil types and showed the highest levels of susceptibility to these oils. Our findings indicate that S. zeamais populations that are resistant to traditional insecticides might have distinct but possibly overlapping mechanisms to mitigate the actions of essential oils and traditional insecticides.

Does cypermethrin affect enzyme activity, respiration rate and walking behavior of the maize weevil (Sitophilus zeamais)?

Insecticides cause a range of sub-lethal effects on targeted insects, which are frequently detrimental to them. However, targeted insects are able to cope with insecticides within sub-lethal ranges, which vary with their susceptibility. Here we assessed the response of three strains of the maize weevil Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae) to sub-lethal exposure to the pyrethoid insecticide cypermethrin. We expected enzyme induction associated with cypermethrin resistance since it would aid the resistant insects in surviving such exposure. Lower respiration rate and lower activity were also expected in insecticide-resistant insects since these traits are also likely to favor survivorship under insecticide exposure. Curiously though, cypermethrin did not affect activity of digestive and energy metabolism enzymes, and even reduced the activity of some enzymes (particularly for cellulase and cysteine-proteinase activity in this case). There was strain variation in response, which may be (partially) related to insecticide resistance in some strains. Sub-lethal exposure to cypermethrin depressed proteolytic and mainly cellulolytic activity in the exposed insects, which is likely to impair their fitness. However, such exposure did not affect respiration rate and walking behavior of the insects (except for the susceptible strain where walking activity was reduced). Walking activity varies with strain and may minimize insecticide exposure, which should be a concern, particularly if associated with (physiological) insecticide resistance.