SUSCEPTIBILITY OF SPODOPTERA FRUGIPERDA (LEPIDOPTERA: NOCTUIDAE) POPULATIONS FROM MARANHÃO, TOCANTINS, PIAUÍ AND BAHIA TO TRANSGENIC MAIZE CULTIVARS WITH CRY/VIP TOXINS FROM BACILLUS THURINGIENSIS

Abstract

In some countries, the use of transgenic maize, cotton and soybean cultivars has increased significantly in recent years, reaching adoption levels above 90% in many regions, imposing intense selection pressure for resistance in the populations of the target insects. The fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), is a polyphagous and migratory insect of global economic importance. Their populations in Brazil represent one of the main targets for the control of insecticidal proteins (toxins) of Bacillus thuringiensis Berliner (Bt) produced in transgenic cultivars. In addition, most of these crops receive applications of synthetic insecticides against a complex universe of insect pests and the adoption of non-Bt refuge areas is low. Several first and second generation Bt corn cultivars (with Cry toxins such as Cry1F, Cry1Ab and Cry1A.105 + Cry2Ab2) have lost efficacy against S. frugiperda populations  by selection for resistance to Bt. Currently, reports lead to the suspicion that S. frugiperda control failures  associated with the resistance event also affect the current third generation Bt corn cultivars,  which jointly produce the toxins Vip and Cry. Although the Vip toxin originally showed efficacy against caterpillars resistant to Cry toxins, at least the caterpillars in the early stages, the loss of efficacy of these toxins makes Bt Vip/Cry corns more vulnerable to Bt resistance selection in S. frugiperda populations. Thus, it is crucial to obtain regional and reliable data on the susceptibility of insect populations to inform decision-making on management practices. The first objective in this study was to investigate the susceptibility status of field populations of S. frugiperda from sites with selection pressure with Bt Vip/Cry corn for more than five years. Time-mortality bioassays were used with F1 descendant third instar larvae from six populations collected in maize fields in the MATOPIBA region, a tropical agricultural frontier that covers four Brazilian states, Maranhão, Tocantins, Piauí and Bahia. The insects were evaluated in longitudinal time-mortality bioassays. The time to death of S. frugiperda third instar larvae  was relatively short, with mortality rates of 98–100% in less than five days, regardless of the Bt corn hybrid containing three combinations of Cry1Ab, Cry1F, Cry2Ab, and Vip3Aa. However, the mean survival time (ST50) of larvae differed between populations, with the lowest and highest ST50 values occurring for the PI-Cr (42 h or 1.75 days) and PI-Ur (66–90 h or 2.75–3.75 days) populations, respectively. Therefore, the third instar larvae of the F1 generation of S. frugiperda populations  were susceptible to corn foliage that produces Vip3Aa/Cry, and the most contrasting susceptibility occurred in insects from the state of Piauí. These results indicate that the progeny of S. frugiperda from areas highly pressured with Bt Vip3Aa/Cry corn hybrids is killed in the corn foliage that produces Bt Vip3Aa and Cry proteins, despite field reports of increased leaf injury by the caterpillars in some localities. In view of these results and the complaints of producers and technicians, the question arose whether there is a change in the susceptibility to Bt toxins in other larval instars of the insect, especially those that are later, supposedly more tolerant to Bt. Thus, the second chapter aimed to investigate whether there is variation in larval survival from the first to the fourth instar of S. frugiperda caterpillars, using the F1 generation of five geographically distinct populations collected in corn fields in the MATOPIBA region. There was a variation in susceptibility in the other instars evaluated, evidenced in the survival curves and mortality after seven days of contact of the larvae with the foliage of Bt corn. The greatest variations and the lowest percentage of mortality were found in the population of Bahia with the fourth instar and in the population of Piauí-Ur in the first and fourth instar and there was heterogeneity in the mortality pattern among the instars depending on the type of Bt corn and the population of the insect. Therefore, no decrease in the susceptibility of the insects was detected in the late instars, reinforcing the general conclusion of susceptibility of the populations collected in the states of MATOPIBA. The results of this study help to understand the risk of evolution of resistance to Vip3A and to refine mathematical models for the sustainable use of Bt crops, an insect management tool that is safe for human health and the environment. Further studies will be needed to investigate the undesirable presence and injury of S. frugiperda in maize crops and to generate tools for the management of S. frugiperda resistance  to Bt maize.