Evolution of Insecticidal Materials for Control of Helicoverpa zea (Boddie)

Helicoverpa zea (Boddie) (formerly in the genus Heliothis) is a major agricultural pest with several common names including corn earworm, bollworm, and tomato fruitworm. The goal of this review is to illustrate the evolution of insecticide chemistries and active ingredients that have been evaluated and developed for H. zea management among key crops, as published in Arthropod Management Tests. Over the past half century, both inorganic and organic insecticides have played a key role in protecting crops from H. zea larvae.

Paris green, an inorganic compound, was an early insecticide used against H. zea and other insect pests. The highly toxic double salt of copper arsenate and copper acetate was first introduced for insect control by French grape growers in the 1870s, and it became the first widespread use of a chemical insecticide in the world by the 1880s (Sorensen 1995). Paris green is not widely used today due to its high toxicity to people, animals, and the environment. By the 1950s and 1960s, organic compounds in the chemical classes of organochlorines, organophosphates, and carbamates were being developed and regularly used to target H. zea in various crops.

Five major events in the United States contributed to the evolution of insecticidal chemistries for H. zea management:

1. Changes in pesticide regulatory law.

   • (A) The Food Quality Protection Act (FQPA), in 1996 amended FIFRA and the Federal Food Drug and Cosmetic Act (FFDCA) fundamentally changing EPA’s regulation of pesticides.

2. Development of resistance among H. zea to various insecticides. The Arthropod Pesticide Resistance Database (2021) lists 17 known active ingredients which H. zea has some degree of resistance.

3. EPA registration and labeling of several transgenic crop plants that produce various crystalline toxins derived from Bacillus thuringiensis.

4. Development of Low- and Reduced-risk Insecticide Chemistries.

5. Increase in organic farming acreage.

Regulatory Changes

The Delaney Clause is a 1958 amendment to the Food, Drugs, and Cosmetic Act of 1938 and the Federal Insecticide, Fungicide, Rodenticide Act (FIFRA), which is the Federal statute that governs the registration, distribution, sale, and use of pesticides in the United States. The Delaney Clause states, ‘…that no cancer-causing agent, as demonstrated in humans or animals, shall be deliberately added to, or found as a contaminant in food’ (Experimental and Toxicologic Pathology, Volume 48, Issues 2–3, February 1996, pages 183–188.). The organochlorine class of insecticides include Aldrin, Chlordane, Dieldrin, DDT, Endosulfan, Endrin, Methoxychlor, and others. Some organochlorine insecticides such as Aldrin, DDT, and Dieldrin are listed as Group 2A carcinogens¹ meaning that they are probable human carcinogens. Although most organochlorine compounds used against H. zea were banned in the 1970s, endosulfan remained in use in U.S. cotton production for bollworm control into the 1992 (Latheef 1993, Klein et al. 1994). Several organochlorine insecticides were used on various crops for H. zea control during the 1970s and 1980s (Berberet 1978, Van Waddill 1979). Organochlorine insecticides are no longer used in the United States due to environmental bioaccumulation hazards and due to their loss during the reregistration process through FIFRA and FQPA.

Insecticide Resistance

Efficacy of organochlorine insecticides against H. zea was beginning to fail due to insecticide resistance in the late 1960s (Plapp 1971, Harris 1972) and soon replaced by the carbamate, organophosphate, and Bacillus thuringiensis (Bt) insecticidal products (Walker and York 1979, Van Waddil 1979, Sorensen 1978, Bacheler and Wilkins 1980, Gardner 1982, McPherson et al.1982, White et al. 1993). Organophosphate insecticides also developed problems with insecticide resistance (Harris 1972, Perez et al. 2000). Shortly thereafter, EPA began to register and label insecticides in the pyrethroid class to replace many of the older organophosphate insecticides for H. zea control (Linduska et al 1983, Pitts and Pieters 1984). Insecticide resistance development has been documented for organophosphate, carbamate and pyrethroid insecticides (Kanga and Plapp 1995). However, some carbamate insecticides (e.g., methomyl) and several pyrethroid insecticides (e.g., bifenthrin, cyfluthrin, esfenvalerate, lambda-cyhalothrin, permethrin, zetacypermethrin) remain efficacious and are still in use for H. zea managment in sweetcorn production (Natwick 2013, Kuhar et al. 2014, Burkness and Hutchinson 2021, Harding and Nault 2021). Acceptance of safer more environmentally friendly insecticides (e.g., Anthranillic dimide, spinosyns) has been retarded by the greater cost per acre, even though these insecticides are equally or more efficacious against H. zea compared with carbamates and pyrethroids.

In recent years, H. zea caused serious losses in many field and vegetable crops throughout the United States. During the 1990s, pyrethroid insecticides became the primary class for managing H. zea. However, in isolated populations of H. zea, signs of resistance to pyrethriod appeared and continued throughout the 1990s–2000s (Abd-Elghafar et al 1993, Kanga et al 1996, Pérez et al. 2000, Pietrantonio et al. 2007, Flood and Rabaey 2007, Hopkins and Pietrantonio 2008, Jacobson et al. 2009).

Development of Transgenic Crops

Transgenic Bt crops evaluated for cotton (Bacheler and Mott 1998, Benedict et al. 1997, Speese 1997) and field corn (Benedict et al 1998, DeLamar et al 2000) production began to greatly reduce reliance on synthetic chemistries for H. zea control during the late 1990s and 2000s. Since the first widely use of transgenic Bt crops in 1996, several insect pests have become resistant to plants that produce a single Bt toxin (Tabashnik et al. 2008). Helicoverpa zea population at various locations have been reported to be resistant to Cry2Ab2 (Yang et al. 2020), Cry1A.105 and Cry2Ab2 (Bilbo et al. 2019), Cry1Ab (Reisig et al. 2018), and Cry1Ac (Anilkumar et al. 2008). With the development of pest resistance to single Bt toxin within crops, industry developed crop plants that produce two or more toxins that kill the potentially resistant pests (Benedict et al. 1999). Farmers in the United States have largely adopted the pyramided or multiple Bt toxin gene strategy, since 2011. Resistance by H. zea to pyramided Bt toxin in cotton was observed and documented in North Carolina (Reisig et al. 2018) and Louisiana (Kaur et al. 2019).

Evolution of Low- and Reduced-Risk Insecticides

Following the passage of FQPA of 1996, the AgriChemical industry quickly responded by developing and marketing several new classes of selective insecticide chemistry as alternatives to OP/carbamates. In general, these products are much safer to use because of their lower mammalian toxicity, reduced impact on pollinators and natural enemies, on nontarget terrestrial vertebrates and on aquatic fauna.

Newer chemistries with activity against H. zea (shown in Table 1) were developed during the mid-1990s through the 2000s (Palmer and Walgenbch 1996, Palumbo 2007, Peters et al 2003, Carson et al. 2009, Herbert et al. 2012). The newer insecticides need to be managed carefully using insecticide resistance management techniques. The newer chemistries such as spinsosyns, diamaides, and others should be used rotation with older insecticidal chemistries to preserve efficacy against a broad spectrum of pests in various cropping systems (Teixeira and Andaloro 2013; Adams 2016; Kund and Trumble 2019).

Increase in Organic Farming

The increased crop acreages cultivated under certified organic farming practices has also contributed to the change in the choice of insecticides for management of H. zea in U.S. crop production (Harding et al 2020a,b). Results from the 2017 Census of Agriculture from the U.S. Department of Agriculture’s National Agricultural Statistics Service (NASS) reported that there were more than 14,000 certified organic farms in the United States in 2016 with farms and ranches sales of nearly $7.6 billion in certified organic goods, more than double the $3.5 billion in sales in 2011. However, the 5 million certified organic acres of farmland in 2016 represent less than 1% of the 911 million acres of total farmland in the U.S. Vermont leads the United States with 11% of its total 1.25 million farm acres as certified organic acres followed by California, Maine, and New York each with about 4% of their total farm acres as certified organic (NASS 2019). A list of USDA Organic Agriculture insecticides with activity against H. zea are included in Table 2.

The reports in the References Cited that are preceded by an asterisk (*) document the changes in insecticidal chemistries used on various crops for H. zea management over the past few decades and can be accessed online in Arthropod Management Tests (formerly Insecticide and Acaricide Tests).

Footnotes

References Cited