CAN TRANSGENIC CROP TECHNOLOGY BENEFIT BIOCONTROL?
Jamie Sutherland & Guy Poppy
Crop plants and insect pests are part of a complex agroecosystem that involves interactions between many trophic levels often referred to as multitrophic interactions1. As such, pest management needs to be viewed from a holistic viewpoint. Because of a lack of harmonization between plant breeders and biocontrol specialists, breeders have continued to strive for total resistance to pests, whilst biocontrol specialists have often ignored the role of the plant in enhancing successful natural enemy foraging behavior. Although some2 have highlighted the need to consider both the bottom-up (plant defense) and top-down (biological control) management of insect pests, there have been too few serious attempts at combining these approaches. As we understand more about the proximate and ultimate function of direct defenses, e.g., allelochemicals, trichomes, etc., and indirect defenses, e.g., recruitment of natural enemies, the potential now exists for genetically engineering plants that can combine both strategies. This article will outline plant traits that may be advantageous to enhancing biocontrol and will summarize how biotechnology could help in this new way of controlling insect pests, which ultimately could stack the odds in man’s favor in his continual ‘war on insect terror’.
Current commercial insect resistant GM plants rely on the production of toxins derived from the bacterium Bacillus thuringiensis (Bt) and, because of Bt’s high pest specificity, are only resistant to a limited number of herbivorous insects. The risks posed by current transgenic plants expressing Bt to biological control agents has already been considered at length in several reviews3,4. This article will explore some of the possibilities that exist for pest management beyond the limitations of expression of Bt in crop plants.
The principal advantage of using GM plants to manage insects is quite clearly the potential for reduced broad-spectrum insecticide inputs. The aim of integrated pest management (IPM) is to become less reliant upon synthetic insecticides, especially as a prophylactic measure. The introduction of Bt varieties has already dramatically reduced the amount of chemical pesticides applied to cotton. In 1998, US cotton farmers used 450 fewer tons of pesticides on Bt cotton than they would have used on conventional varieties. Naturally, reduction in the use of insecticides should have immediate benefits for biocontrol by allowing greater numbers of parasitoids and predators to survive. This has been seen in China where GM cotton has a significantly higher abundance of parasitoids and predators than conventionally sprayed cotton.
Rather than depend solely on crop plants that confer insect resistance by the production of Bt toxins, can we use and enhance the plant’s direct and indirect defenses to enhance biological control? It is probable that conventional breeding of many of our crop varieties in the past has bred out many traits that could be beneficial to natural enemies, whether indirectly or directly. We will discuss some of these here, citing several examples where conventional plant breeding has had significant direct and indirect effects on the fecundity, mortality, and behavior of natural enemies.
The use of biocontrol in arable crops has had limited success because of the problem of attracting and maintaining a high enough density of parasitoids and/or predators in the crop. Host-plant volatiles have an important role in attracting natural enemies, so by manipulation of the host-plant chemistry it could be possible to attract predators and parasitoids to their prey and hosts. Cotton is an often cited example of this phenomenon in which attack by herbivorous insects induces plant signals for their corresponding parasitoids. Naturalized (wild) cotton plants can produce many more signal volatiles than commercial varieties, but traditionally breeding wild cotton with modern cultivars has proved problematic. In the future, it may be possible to genetically engineer this pathway into modern cotton cultivars.
Terpenoid compounds are also believed to play an important role in attracting natural enemies. Corn plants may release large amounts of terpenoid volatiles after damage by beet armyworm (Spodoptera exigua). Plants that were artificially damaged did not release these volatiles in significant amounts unless saliva from the caterpillars was applied to the damaged sites. Females of a parasitic wasp (Cotesia marginiventris) also use these same plant-derived volatiles to locate their hosts5.
It should be noted that the effects of enhanced allelochemical production on natural enemies are not always beneficial. Negative effects of enhanced glucosinolate production in some brassica crops have been reported. Higher glucosinolate concentrations caused an increase in mortality of ladybird larvae when feeding on aphids. This does, however, demonstrate the importance of plant allelochemicals on third trophic levels and should be borne in mind when considering plant manipulation, whether by genetic modification or by conventional breeding.
Permanent expression of plant signals, which attract parasitoids or predators, in the plant is to be avoided. Natural enemies, in particular parasitoids, have remarkable powers of learning and are likely to quickly gain the knowledge that a plant that is producing a particular allelochemical, yet has no host or prey associated with it, is unprofitable and will learn to utilize more successful cues. It is probably more appropriate to use external chemical signals to switch on plant genes6. Finally, it is important to remember that because of the great genetic diversity in parasitoid populations and phenotypic plasticity of individuals, there is often a substantial variation in the response to chemical cues. The successful utilization of enhanced allelochemical-parasitoid systems will require careful management of these intrinsic parasitoid parameters.
By looking at the achievements of conventional breeding for resistance to pests, we can also begin to understand the possibilities and limitations of using transgenes to confer resistance. Perhaps there is a potential for compatibility of partial plant resistance with biocontrol. One notable example in which this was certainly not the case was in a partially resistant wheat cultivar (with conventionally bred resistance). The size of the aphid population (Metopolophium dirhodum) feeding on the wheat was reduced by 5%, but the knock-on effects of this on the third trophic level was a 34% size reduction in the aphid’s parasitoid population (Aphidius rhopalosiphi). This was due largely to increased restlessness of the aphids on the partially resistant wheat cultivars. Again, this demonstrates the complexity of and the need for investigating effects on third and possibly even fourth trophic levels.
Morphological traits in plants, such as trichomes, waxiness, and toughness, can also positively or negatively influence natural enemy behavior, and these traits could also be genetically engineered into plants. Most of the examples cited in the literature describe only the negative effects on natural enemies. For example, leaf hairiness can adversely affect parasitoid searching behavior in tobacco, potato, and cotton crops. Cabbage varieties with increased leaf waxes can also affect the mobility of generalist predators such as lacewings (Chrysoperla carnea) because the waxes accumulate on the tarsi of these insects. A large number of potentially valuable morphological traits may have been inadvertently bred out of modern crop cultivars but, by looking at wild crop relatives and their effects on natural enemies, we can perhaps select those traits that are beneficial to natural enemies and reinsert those genes into the crop cultivars.
Adult parasitoids and some predators tend to rely on an alternative food source for their larvae, and this is usually in the form of floral nectar, extrafloral nectar, pollen, and honeydew. Genetic modification of crop plants could be utilized to increase the production of resources for natural enemies to enhance biological control. A classic example from cotton, in which the resource requirements of parasitoids were ignored, occured when crop varieties were bred without extrafloral nectaries. This was done to prevent sooty mould formation on the developing bolls. This nectariless cotton actually had increased bollworm (Helicoverpa zea) damage due to a lack of parasitoids in the field. The adult parasitoids had previously been utilizing the nectar as a food resource7.
As we enter the post-genomic era, manipulating plants to assist natural enemies will become technically possible. Many of the scientific solutions we have suggested above are already feasible by conventional means, and soon all will become possible by transgenic technology. Use of this novel technology will permit a more rapid transfer of technology to the end user, i.e., the farmer. Previously, conventional breeding for insect resistance in a crop has proved to be a hit and miss affair. This has invariably meant exposing thousands of breeding lines to the pest and scoring their level of innate resistance. Evidently, this is a highly labor intensive process, although there have been some notable successes, e.g., the brown plant hopper, (Nilaparvata lugens)—the major pest in Asian rice. The impact of resistance on biological control should be examined carefully, particularly if it has been achieved through transgenic technology. It is vital that the environmental risks are fully assessed using robust risk assessment protocols to reduce the potential for severe disruption to ecological systems and their interactions. GM crops do have the potential to benefit biological control and to become a vital tool in any IPM program.
References
1. Poppy GM (1997) Endeavour 21: 61-65
2. Cortesero AM, Stapel JO, Lewis WJ (2000) Biol. Control 17: 35-49
3. Groot AT, Dicke M (2002) Plant J. 31: 387-406
4. Poppy GM, Sutherland JP (2004) Physiol. Entomol. 29: 257-268
5. Turlings TCJ et al. (1995) Proc. Natl. Acad. Sci. USA 92: 4169-4174
6. Pickett JA, Poppy GM (2001) Trends Plant Sci. 6: 137-139
7. Treacy MF et al. (1987) Environ. Entomol. 16: 420-423
Jamie Sutherland & Guy Poppy
Ecology and Evolutionary Biology
Southampton, United Kingdom
jps4@soton.ac.uk

IMPACT OF Bt COTTON ON BOLLWORM POPULATIONS AND EGG PARASITISM
Mellet MA & Schoeman AS
Transgenic cotton or Bt cotton, i.e., cotton that contains δ-endotoxin genes (cry genes) from Bacillus thuringiensis Berliner var. kurstaki, was introduced to combat Heliothis virescens and Heliothis zea (Lepidoptera: Noctuidae) in the U.S. Bt cotton is lepidopteran specific and symptoms of δ-endotoxin protein ingestion include midgut paralysis, altered permeability and disintegration of the midgut epithelium, as well as an altered pH in the midgut. Insects thus stop feeding, become dehydrated, and ultimately die. The cultivation of Bt cotton, therefore, allows the producer to use fewer insecticide sprays during integrated pest management programs where susceptible bollworm species are a problem.
Helicoverpa armigera (Hübner) bollworm (Lepidoptera: Noctuidae) is one of the major agricultural pests in South Africa. Reports on Bt cotton efficacy against H. armigera are few and vary in the degree of control achieved. Damage to cotton plants is characterized by feeding activity on squares (flower buds), flowers, and cotton bolls, which results in shedding of these reproductive plant parts. This may lead to a loss in yield when it occurs ten weeks after plant emergence.
Development of resistance to Bt toxins is possible. Laboratory H. armigera populations developed resistance to Bt cotton within six to seven generations after first exposure1. The use of refuges relying on a high dose strategy has been proposed to delay the development of resistance in bollworm populations. Five percent of cotton fields must be non-Bt and not sprayed, or 20% of cotton fields must be non-Bt and may be sprayed with agrochemicals other than microbial sprays. Oviposition preference of susceptible female moths for non-Bt cotton might slow down the development of Bt resistance, as more eggs will be laid in refuge areas, with fewer larvae being exposed to Bt. Oviposition preference by H. armigera females has not been evaluated.
A decrease in insecticide use in Bt cotton fields can increase beneficial arthropod diversity and abundance in these fields. Bt cotton has a narrow efficacy range and no direct negative impact against natural enemies can be expected. But it is still possible that beneficial arthropods might be indirectly influenced by the presence of the Bt gene. The behavior of non-target organisms or consumption of prey that survived the uptake of Bt toxin could play a role in how the population will be affected by Bt crops. For example, the egg parasitoid Trichogrammatoidea lutea Girault (Hymenoptera: Trichogrammatoidea) might be indirectly influenced through changes in its behavioural patterns, i.e., the females change their oviposition patterns to avoid laying eggs in Bt cotton fields.
Trichogrammatoidea lutea kills the developing H. armigera embryo inside the egg and plays an important role in IPM (integrated pest management) tactics in which biological control is involved. If Bt toxins produced by Bt cotton do not pose direct and indirect threats to T. lutea, then Bt cotton can play an important role in the application of biological control.
A two-year field study was conducted at Marble Hall, South Africa, to determine the efficacy of Bt cotton against H. armigera and the effect thereof on egg parasitism by T. lutea and Telenomus ullyetti Nixon (Hymenoptera: Scelionidae)2. Helicoverpa armigera oviposition and larval and adult abundance were determined in Bt cotton (NuOpal) and non-Bt cotton fields (Delta Opal; referred to as control) using the scouting method. A sprayed non-Bt cotton field was included during the second season. Funnel-type pheromone traps, baited with H. armigera sex pheromone, were used to determine the number of adults in the cotton fields. Bollworm eggs were collected from the field during the second season and kept in a laboratory to determine the number of eggs from which parasitoids emerged.
Bt cotton effectively controlled H. armigera during both seasons and no insecticide applications were necessary at any stage of plant development within the Bt cotton fields. The highest number of eggs and larvae were found during the flowering and boll-forming stages of the cotton plants in the control field. The threshold level of H. armigera larvae, as indicated by the ARC – Tobacco and Cotton Research Institute3, is five larvae per 24 plants. Larval numbers per 24 plants were as high as 19.2 in the control, in contrast to only 1.6 larvae found on Bt cotton during the second season (Table 1).