Diamide seed treatment may protect early soybean growth stages against Helicoverpa armigera
Graphical abstract
Helicoverpa armigera can compromise soybean crop establishment in intensive systems. Soybean seed treatment with chlorantraniliprole or cyantraniliprole is potentially efficacious against noctuid larvae in the first 14 days (VE-–V1 soybean growth stages), causing lethal and sublethal effects on the insects.
Introduction
Insects are one of the main factors causing losses in food and fiber production, especially in agricultural landscapes with intensive cropping systems of soybeans, maize, or cotton (Oerke, 2006; Oliveira et al., 2014). Helicoverpa armigera, the Old World bollworm, is a major global lepidopteran pest in many field, fruit, and horticultural crops (Cunningham and Zalucki, 2014). In the Western Hemisphere, the insect was first officially recorded in Brazil in 2013 (Czepak et al., 2013; Specht et al., 2013; Tay et al., 2013), and then in Argentina and other South American countries and Puerto Rico (Kriticos et al., 2015; Murúa et al., 2014). The intensive (sub)tropical agricultural production in its new geographical range favors the pest status of the Old World bollworm, aided by its remarkable polyphagy, multivoltinism, population growth potential, and predisposition for insecticide resistance (Kriticos et al., 2015). In 2020, out of the 350 million tons of soybeans produced globally, 52% were from South America (mostly Brazil, Argentina, Paraguay, and Uruguay) (FAOSTAT, 2022; Klein and Vidal Luna, 2021; Song et al., 2021). In the region, during early soybean growth stages, bollworm larvae can consume the leaves, apical growth points, and axillary shoots, reducing stand or compromising plant capacity for growth and damage compensation (Rogers and Brier, 2010). This species and other noctuid larvae thrive on the reproductive structures (flowers and pods) of soybean, cotton and other host plants (Czepak et al., 2013; Fathipour and Sedarati, 2013; Haile et al., 2021). Thus, effective control measures are critical to protecting soybeans against noctuid larvae (Páez Jerez et al., 2022).
Transgenic soybean varieties expressing the Cry1Ac Bacillus thuringiensis (Bt) insecticidal protein have been widely adopted in over 60% of the crop acreage in South America, but additional synthetic insecticide applications may be needed to control noctuid larvae of Helicoverpa and Spodoptera spp. (Bernardi et al., 2014; Páez Jerez et al., 2022Rabelo et al., 2020a, Rabelo et al., 2020b). While second-generation Bt soybean producing two (Cry1Ac + Cry1F) or three (Cry1Ac + Cry1A.105 + Cry2Ab2) Bt insecticidal proteins have recently been introduced (Bacalhau et al., 2020; Marques et al., 2017), there is also the threat that their efficacy against the bollworm is diminished as resistant populations may readily be selected when management strategies are not effectively used (Luttrell et al., 1999; Rabelo et al., 2020c; Pereira et al., 2020; Abbade-Neto et al., 2022; Walsh et al., 2022). In addition to soybean, Bt cultivars of maize and cotton are widely used in the region, especially in Brazil, and provide selective control of major lepidopteran pests. Whereas cases of resistance to Cry1Ac Bt soybean have not yet been reported for its primary targets, including H. armigera, unexpected damage by looper larvae (Rachiplusia nu) was detected in Brazil and Argentina in 2021/2022 (Horikoshi et al., 2021; Páez Jerez et al., 2023). These issues, along with the current prospects of human population growth, require growers to adopt integrated solutions to manage pests like the Old World bollworm and sustain the basis of our food and fiber production systems (Fathipour and Sedarati, 2013; United Nations, 2019).
Seed treatment may be useful to help protect the most susceptible soybean growth stages, typically early in the season (Hesler et al., 2018; Papiernik et al., 2018). As for many field crops, managing bollworm infestations using foliar sprays when plants are small can be difficult because spray coverage is often inadequate and efficacy is limited (Pes et al., 2022; Nault et al., 2004). Compared with foliar applications, seed treatment can require less pesticide to control pests, thereby reducing exposure to the insecticide for the user and the environment, but not without unintended effects (Hitaj et al., 2020; Krupke and Tooker, 2020; Mourtzinis et al., 2019; Nault et al., 2004; Pedrini et al., 2017; Vojvodić and Bažok, 2021). Seeds can be treated with a contact insecticide to control underground insect pests, but a systemic compound is needed against aboveground targets. The active ingredient must have suitable water solubility and lipophilicity for sufficient intake and upward movement in the plant (Cloyd et al., 2011). This process occurs through the plant vascular system driven by the transpiration flow (Barry et al., 2015; Pes et al., 2020, Pes et al., 2022 Zhang et al., 2018, 2019), and the translocation rates can depend on the plant species, its age, and environmental and physiological conditions (Cloyd et al., 2011).
There are several classes of insecticides active against lepidopterans in field crops, including diamides (Oliveira et al., 2022; Pes et al., 2020), which are modulators of insect ryanodine receptors (IRAC, 2021). Introduced in the late 2000s (Jeanguenat, 2013), such compounds target pests in many crops worldwide (Adams et al., 2016). Formulations of chlorantraniliprole and cyantraniliprole are registered for seed treatment and foliar application. The former insecticide was the first anthranilicdiamide introduced against lepidopterans and other chewing insects (Lahm et al., 2009; Selby et al., 2017). Cyantraniliprole has a broader spectrum of action, including insects in Lepidoptera, Diptera, Coleoptera, Hemiptera, and Thysanoptera (Foster et al., 2012). Additionally, neonicotinoid and carbamate insecticides, which act as acetylcholine agonists or acetylcholinesterase inhibitors, respectively, continue to be widely used to control hemipterans, lepidopterans, and sometimes coleopterans (Renkema et al., 2015) and nematodes. These compounds were introduced much earlier, with carbofuran (carbamate) in the 1960s and imidacloprid (neonicotinoid) in the 1990s (Abreu-Villaça and Levin, 2017; Casida and Durkin, 2013).
Crop protection against arthropod pests is primarily accomplished through the lethal and sublethal effects of pesticides on the target organism (Guedes et al., 2016), and assessing these pesticides in controlled conditions help understand their potential implications for pest management. Sublethal effects are defined as any physiological, demographic, or behavioral effects on individuals surviving exposure to a toxicant and can impact the life span, developmental rates, metamorphosis, sex ratio, fecundity, fertility, population growth, and more. The systemic insecticide concentration is expected to decay with time as a result of the distribution, metabolization, or degradation of active ingredients in the plant and the external environment (Cutler et al., 2022; Magalhães et al., 2009). The declining insecticide concentrations may cease to cause insect mortality, but they may change individual traits that can reduce or increase the potential for population growth (Cutler et al., 2022; Guedes et al., 2016), thus mattering for predicting the window of crop protection (Magalhães et al., 2009; Oliveira et al., 2022).
In this study, we assessed the potential of systemic insecticides applied to soybean seeds for plant protection against a noctuid pest, the residual efficacy period, and sublethal post-exposure effects on the insect life history and population fitness. Our hypotheses were that: 1) some insecticide seed treatments are effective against the noctuid larvae during the early vegetative stages of soybeans; 2) newer and more selective compounds such as the diamides provide intended effects greater than traditional insecticides introduced two–four decades ago, and 3) sublethal effects of seed treatment depend on the active ingredient, its mode of action, and time after plant emergence. We discuss which systemic insecticide seed treatments in soybeans may be appropriate according to the targets and the situation.
Section snippets
Insects
Helicoverpa armigera eggs were obtained from PROMIP supplier (Limeira, São Paulo, Brazil) and maintained in the Insect-Plant Interaction Laboratory of the Federal University of Viçosa (UFV), Minas Gerais, Brazil. After hatching, the neonates were transferred to 500-mL plastic containers with an artificial diet (Greene et al., 1976). After reaching the third instar (1–1.5-cm size), to avoid cannibalism, the larvae were placed individually in 16-well polyvinylchloride trays (Advento plastics,
Plant protection and larval mortality
Plant growth stage and seed treatment conditioned the leaf area consumed by the larvae (Table 2, P < 0.05), and we fitted non-linear regression models to understand the interaction (Fig. 1a, Table 3). The percentage of leaf area consumed by the larvae on control plants was close to 80% during the first ten days after plant emergence. The larvae consumed 40–55% of the leaf area of plants seed treated with carbofuran, an intermediate plant protection effect compared to the control (80%
Discussion
The potential for plant protection, residual efficacy, and sublethal effects on targeted insects are fundamental information to predict the utility of seed-applied insecticides and performance for crop protection. Here, consistent with our hypotheses, chlorantraniliprole and cyantraniliprole caused more than 80% larval mortality and reduced plant damage for approximately 14 days after soybean emergence, thus showing high potential to be effective via seed treatments against early-season attacks
Main findings in one sentence
Systemic diamide insecticide seed treatment may help manage Helicoverpa armigera by causing lethal and sublethal effects on the insects and efficaciously protecting soybean plants for 14 days after emergence.
CRediT author statement
Paula Páez Jerez: Investigation, Data curation, Writing- Original draft preparation, Project administration.
Antônio Carlos Alves: Methodology, Investigation.
Johana Quinteros: Investigation.
Leidiana Ribeiro: Visualization, Investigation.
Jorge Hill: Software, Writing - Review & Editing.
M Teresa Vera: Supervision, Funding acquisition, Writing - Review & Editing,
Mateus Gonzato: Resources, Writing - Review & Editing.
Rafael Pitta: Supervision, Writing - Review & Editing.
Eliseu Pereira:
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We thank the research assistants in the Laboratory of Insect-Plant Interaction for assisting in insect rearing, plant cultivation, and data collection. The soybean research team working in the Agronomy Department with Prof. Felipe Lopes provided the soybean seeds. The following Brazilian funding agencies provided financial support: CNPq (Ministry of Science, Technology, and Innovation), CAPES (Ministry of Education, Finance Code 001), and FAPEMIG (Minas Gerais State Foundation of Research Aid).
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