Use and Impact of Bt Maize

Most people are familiar with the hungry caterpillar in the vegetable garden or the elusive beetle in the pantry, and contending with these unwelcomed pests is a longstanding problem. Ever since humans started farming they have shared part of their harvest with insects. Growers of maize, Zea mays (corn), are challenged with a number of pests, but the most important are lepidopteran larvae (i.e., caterpillars) that are stalk borers, ear or leaf feeders, and coleopteran larvae (i.e., beetle grubs) that feed on roots. The European corn borer, Ostrinia nubilalis, for example, was nicknamed the "billion dollar bug" because it cost growers over a billion dollars annually in insecticides and lost crop yields (Figure 1). Most maize growers rely on traditional crop protection practices to manage these insects, including cultural, biological or chemical (insecticide) methods or a balance of these methods that aims to minimize environmental impact called integrated pest management (IPM) (Hellmich et al. 2008). However, in 1996 USA growers were introduced to commercial maize that was genetically engineered (GE) with resistance to European corn borer and other lepidopteran maize pests. In 2003 another GE maize was introduced that killed corn rootworm larvae (beetle grubs), especially larvae of the western corn rootworm, Diabrotica virgifera virgifera, another "billion dollar bug" (Figure 2). These GE plants produce crystal (Cry) proteins or toxins derived from the soil bacterium, Bacillus thuringiensis (Bt), hence the common name "Bt maize". Bt maize has revolutionized pest control in a number of countries, but there still are questions about its use and impact. This article will focus on the opportunities and challenges presented by Bt maize as they relate to current insect-resistant products.

Bacillus thuringiensis is a species of bacteria that produces proteins that are toxic to certain insects. Because of this, it has been used as a safe microbial insecticide for over 50 years to control pest caterpillars. Bt insecticides are popular with organic farmers because they are considered "natural insecticides" and they differ from most conventional insecticides because they are toxic to only a small range of related insects. This is because specific pH levels, enzymes, and midgut receptors are required to activate and bind a given Cry toxin to midgut cells, which leads to pore formation in the insect's intestine and death (Federici 2002). A "lock and key" analogy is useful to explain this specificity. If the midgut receptor is considered the "lock" and the Cry protein is the "key" then insect death only occurs when the "lock and key" match.

There are a number of Cry toxins that are categorized by their spectrum of activity. For maize pests, primary Cry proteins are Cry1 and Cry2 for Lepidoptera and Cry3 proteins for Coleoptera (Schnepf et al. 1998). Maize can be genetically engineered to produce these specific Cry toxins. As such, aspects of Bt maize are similar to host plant resistance traits such as DIMBOA (2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one), which at high levels reduces damage by European corn borer (Klun et al. 1967). Seed providers often combine or stack traits for Lepidoptera and Coleoptera control into the same plant. Also, different types of Bt toxins targeted for the same insects are often combined into more effective plant protectants called pyramids. This multiple toxin approach is useful for managing insect resistance to Bt maize.

Growers are attracted to the convenience of Bt maize hybrids because they allow for "in the bag" insect protection. GE maize seed comes from the seller with innate pest resistance. Functionally, this means that growers will be handling and applying fewer chemical insecticides, which has both health benefits for the growers and important environmental benefits. It also of course means farmers can spend less time applying insecticides but still be confident in the protection of their crop from key pests. Furthermore, growers are attracted to the yield protection and improved grain quality commonly found with Bt maize. Interestingly, due to the introduction of Bt maize, recent research suggests there has been an areawide suppression of European corn borer populations (Hutchison et al. 2010). This is beneficial to both Bt and non-Bt maize growers.

Bt maize offers both economic and environmental advantages and grower responses indicate an awareness of both types of these benefits. Many growers cite unique opportunities to protect yield and reduce handling (and use) of insecticides to explain their rapid adoption of Bt maize (Pilcher et al. 2002). Brookes and Barfoot (2010) estimated that from 1996 to 2008 the cumulative decrease in insecticide active ingredient (a.i.) use on Bt maize was 35% (29.9 million kg) globally. Much of the reduction in insecticide a.i. was probably due to coleopteran-active Bt maize, as insecticides used against Diabrotica spp. comprise 25–30% of the global total in maize (James 2003, Rice 2004).

Historically, growers had difficulty controlling corn borers because insecticides are not effective after larvae have tunneled into the stalk. One entomologist called corn borers "silent thieves" because stalk tunneling and ear injury often reduced yields 5-10 percent or more with many growers not even noticing. When entomologists started to experiment with Bt maize in the early 1990s, many were astounded that the plants were nearly "bullet proof" to corn borer injury. Previously plant breeders were able to increase host plant resistance, but none of these plants were "bullet proof". Not surprisingly, growers that use Bt maize often see higher yields due to this reduced insect injury (Gómez-Barbero et al. 2008).

Another benefit of Bt maize is reduced occurrence of ear molds (Figure 1b). Because insect damage provides a site for infection by molds, Bt-protected maize can have lower levels of toxins produced by molds (i.e., mycotoxins), especially fumonisin and deoxynivalenol (Dowd 2000, Munkvold et al. 1999). Consequences of contamination with mold may be serious, as fumonisins can cause fatal leukoencephalomalacia in horses, pulmonary edema in swine, and cancer in laboratory rats. Economic analysis suggests that USA farmers save $23 million annually through reduced mycotoxins (Wu et al. 2004) and mycotoxin reduction also could be a significant health benefit in other parts of the world where maize is a diet staple (Wu 2006).

Detractors of Bt maize suggest several challenges, including the potential for effects on non-target organisms and gene flow between Bt maize and non-Bt maize, to outweigh any benefits. Other issues to consider include whether insect resistance to Bt toxins can be managed, and whether the use of Bt maize is compatible with the other pest control methods.

There have been no surprising effects on non-target organisms observed with Bt maize, which confirms the specificity of the Bt proteins. Most studies suggest Bt maize has little if any impact on predators and parasitoids and, when compared with maize treated with chemical insecticides, Bt maize often results in increased biodiversity [for general reviews see (O'Callaghan et al. 2005, Romeis et al. 2008)]. Specialist insects that depend on target pests are the exception to the generalization that Bt maize does not impact non-target organisms. This is particularly true for some parasitoids, which may become less abundant along with their herbivorous hosts (Pilcher et al. 2005, Romeis et al. 2008, Storer et al. 2008). Also, fewer saprophagous dipterans (i.e., fly larvae that feed on decaying organic matter) have been observed in Bt maize fields, which has been attributed to the indirect effect of reduced lepidopteran plant injury (Candolfi et al. 2004, Dively et al. 2004). Studies with monarch butterfly caterpillars, Danaus plexippus, suggested monarch butterfly populations would be reduced from feeding on milkweed leaves coated with Bt maize pollen (Jesse & Obrycki 2000, Losey et al. 1999). Follow-up studies, however, indicated that the impact was negligible because of limited exposure and low toxicity of Bt maize pollen to monarch caterpillars (Dively et al. 2004, Hellmich et al. 2001, Sears et al. 2001, Stanley-Horn et al. 2001).

The transfer of genetic material between populations (i.e., gene flow) is often considered to be a potential problem between GE crops and their wild relatives (Messeguer 2003). In most areas of the world producing GE maize, however, production is isolated from related species that could hybridize with maize. Therefore, this environmental concern is restricted to areas where wild relatives of maize occur (e.g., Mexico). Maize is an open-pollinated crop, but the large size of pollen grains limits its movement. Nonetheless, some growers, particularly organic growers, demand little or no contamination from GE pollen or seed and generally object to production of any GE maize. This has been a particularly controversial issue in Europe.

Successful control of insects by Bt maize has many scientists concerned that overuse of Bt maize could produce pests resistant to Bt toxins. Field-evolved resistance to Bt maize has occurred for two moth species: fall armyworm, Spodoptera frugiperda, in Puerto Rico, and African stem borer, Busseola fusca, in South Africa, so this concern is warranted. Various strategies have been proposed for managing insect resistance to Bt maize, but currently the high-dose/refuge (HDR) strategy is the most commonly recommended (Bates et al. 2005, Tabashnik 1994). With this strategy, insects that feed on the Bt maize are exposed to an extremely high dose of toxin; and this is complemented with refuges, usually non-Bt maize, that provide a population of susceptible insects that are not exposed to Bt toxin (Figure 3). Consequently, rare resistant moths that develop on Bt maize, instead of mating with each other, mate with individuals among the overwhelming number of susceptible moths from the refuge (Gould 1998, Tabashnik & Croft 1982). This process essentially dilutes resistance genes and maintains a population of susceptible insects. The HDR strategy should be effective as long as plants express a high dose of the toxin, genes conferring resistance are rare, and there are many insects from the refuge available to mate randomly with resistant insects (Gould 1998). Sometimes convincing growers to plant non-Bt maize refuges is a challenge because it requires careful planning of where to plant the refuge and could reduce yields. Currently in the USA refuge recommendations range from 5–20 percent, depending on region of the country and type of Bt maize.

Pyramided maize that produces two Bt proteins with different modes of action targeted for the same insect has reduced refuges because the two-toxin "redundant killing" reduces the chances that insects will evolve resistance. A challenge with the HDR strategy is Bt maize is not high dose for many common maize pests. For example, lepidopteran Bt maize is not high dose for fall armyworm, S. frugiperda, corn earworm, Helicoverpa zea, and cutworm species (family Noctuidae), while coleopteran Bt maize is not high dose for corn rootworm (Diabrotica spp.). Both instances of field resistance, fall armyworm, S. frugiperda, in Puerto Rico, and African stem borer, B. fusca, in South Africa, involved species that were only moderately susceptible to Bt maize. But it is unclear if resistance evolution was due to lack of high dose or insufficient refuge.

Although Bt maize is an important tool for growers, it cannot completely replace other pest control tactics. Insecticides, for example, may be necessary to control secondary insect pests. Host plant resistance is important to maintain because if pests become resistant to Bt toxins it will be needed as a backup method of pest control. Finally, Bt maize should be especially compatible with biological control because reduced use of insecticides should lead to an increase in beneficial insects (Naranjo 2009). In general, traditional pest management practices must be maintained in order to avoid reliance on a single tactic.

Active ingredient: Substance in a pesticide that is biologically active.

Biological control: Control of a pest by the introduction of a natural enemy (predator, parasite or pathogen).

Coleoptera: The insect order comprising beetles.

Crystal (Cry) proteins: Proteinacous inclusions produced by many strains of Bacillus thuringiensis during spore formation that have insecticidal activity.

Cultural control: Management techniques used in agricultural to reduce pest populations, such as crop rotation.

Deoxynivalenol: Mycotoxin produced by the fungus Fusarium graminearum and other fungi that occurs mainly in grains such as wheat, barley, oats and maize, also known as vomitoxin.

DIMBOA (2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one): Naturally occurring compound (hydroxamic acid) present in maize and other related grasses that serves as a defense against insects, fungi and bacteria.

Entomologist: Person who studies insects.

European corn borer: Stem-boring insect native to Europe that was accidently introduced into North America in the first decade of the 20th century. Larval stage is a pest of grain, particularly maize.

Fumonisin: Toxins produced by species of Fusarium molds that frequently occur in maize and other crops. Certain types are harmful to humans.

Gene flow: Transfer of genes from one population to another within the same species.

Genetic engineering: Insertion of a modified gene or gene from another organism using various recombinant DNA methods.

High-dose/refuge strategy: Tactic used to delay insect resistance to a genetically modified (GM) crop that involves planting non-GM plants (refuge) to produce susceptible insects. In order for the strategy to be effective the toxin dose in the plant must be sufficiently high to kill offspring derived from susceptible and resistant insects (i.e., heterozygous individuals).

Host plant resistance: Natural defenses plants evolved to reduce the impact of herbivores. Plant breeders often select these traits to reduce losses due to pests.

Insect resistance: Many insects have evolved resistance to insecticides, which can result in crop failures. Likewise insects can evolve resistance to GM plants.

Integrated pest management: A pest management strategy that uses a variety of methods usually biological control, host plant resistance, cultural control, and minimal use of pesticides to control crop pests.

Lepidoptera: An order of insects that includes butterflies and moths.

Leukoencephalomalacia: Disease of the central nervous system that affects horses, mules and donkeys, commonly called "Moldy Corn Poisoning".

Mycotoxins: A toxin produced by a fungus.

Natural insecticides: An insecticide produced from plant extracts, e.g., pyrethrum is produced from the flower chrysanthemum.

Open-pollinated: Pollination occurs by natural mechanisms such as insects, birds or wind. Maize is wind pollinated.

Plant pyramid: Plants with two or more Bt toxins targeted against the same pest.

Pulmonary edema: Abnormal build up of fluid in air sacs of lungs.

Western corn rootworm: A beetle from the family Chrysomelidae that is a major pest of maize in the United States. The main economic damage occurs when larvae feed on maize roots that can lead to plant lodging, harvesting difficulties and yield loss. In 1992 this beetle was discovered in Europe.