George G. Kennedy

Integration of Insect-Resistant Genetically Modified Crops within IPM Programs

Although host plant resistance has long been an important insect management tactic, its wide-spread use has been constrained by the limited availability of elite cultivars possessing high levels of resistance to key pest species. The application of recombinant DNA technology to genetically engineer insect-resistant crop plants has provided a way to eliminate this constraint and make host plant resistance a prominent component of integrated pest management (IPM) in major cropping systems world-wide. It is within the framework of IPM, rather than as a stand-alone insect control measure, that insect-resistant GM crops have the greatest potential to contribute to the establishment of sustainable crop protection systems. This chapter reviews the defining elements of IPM and examines the attributes of insect-resistant GM crops as IPM tools. Insect-resistant GM crops available to date, like their counterparts developed through conventional plant breeding, are proving to be safe, effective and easy to use insect suppression tools that are compatible with other IPM tactics, including cultural and chemical controls and the conservation of natural enemies as important agents of biological control. Because of their high level of efficacy against the key pest species that they target, GM Bt cotton and Bt maize varieties expressing cry genes derived from Bacillus thuringiensis (Bt) have been widely adopted and have led to significant reductions in insecticide use. Experience in Bt cotton has revealed the potential for reductions in insecticide use to be accompanied by the emergence of secondary pests and the need to adjust the pest management systems to address these “new” pests. Emphasis on the importance of resistance management to mitigate selection for pest adaptation to Bt crops has elevated the role of resistance management to a position of fundamental importance in the implementation of IPM.

2-Tridecanone: A Naturally Occurring Insecticide from the Wild Tomato Lycopersicon hirsutum f.glabratum

A nonalkaloid insecticide was isolated from the wild tomato Lycopersicon hirsutum f. glabratum and identified as 2-tridecanone, a compound 72 times more abundant in the wild tomato than in the cultivated tomato L. esculentum. Lepidopterous larvae (Manduca sexta and Heliothis zea) and aphids (Aphis gossypii) died when confined on 2-tridecanone-treated filter paper.

Effects of natural enemies on the rate of herbivore adaptation to resistant host plants

The potential of natural enemies to influence the rate of herbivore adaptation to resistance factors in plants is examined using conceptual and mathematical models. Results indicate that natural enemies could increase or decrease the rate of herbivore adaptation. The specific behavioral and physiological effects of a resistance factor on the herbivore, as well as the behavior of the natural enemy, and the population dynamics of the natural enemy/herbivore system are important in assessing the extent to which the natural enemies will affect the rate of herbivore adaptation to a resistance factor. Herbivore adaptation to partial resistance in a host‐plant is generally expected to be slower than adaptation to high levels of resistance, even in the presence of natural enemies, if genetic variance is not limiting.

THE ROLE OF GLANDULAR TRICHOMES IN THE RESISTANCE OF LYCOPERSICON HIRSUTUM F. GLABRATUM TO HELIOTHIS ZEA

Removal of the glandular trichome exudate from leaflets of the wild tomato Lycopersicon hirsutum f. glabratum PI 134417 by swabbing with ethanol resulted in loss of resistance to larvae of the tomato fruitworm (Heliothis zea). An extract containing the exudate and little else was toxic to first‐instar fruitworm larvae. Gas chromatographic analysis of extracts containing only the excised tips of the glandular trichomes revealed the presence of 2‐tridecanone, a compound toxic to H. zea and other arthropods. The toxin was found to be nearly absent from the leaflet interior, being present in significant quantities only in extracts of leaflet surfaces. H. zea larvae were killed by fumes from the surface extract and from pure 2‐tridecanone. The air surrounding PI 134417 leaflets was found to be rich in 2‐tridecanone vapors. Fumigant action is a major avenue of their exposure to 2‐tridecanone on the foliage of PI 134417. While larvae are quickly immobilized by fumes when placed on resistant leaflets, most recover within 24 hr, casting doubt on 2‐tridecanone as the sole defensive compound in PI 134417 against H. zea.

Overwintering of Frankliniella fusca (Thysanoptera: Thripidae) on Winter Annual Weeds Infected with Tomato spotted wilt virus and Patterns of Virus Movement Between Susceptible Weed Hosts.

ABSTRACT Overwintering of tobacco thrips, Frankliniella fusca, was investigated on common winter annual host plants infected with Tomato spotted wilt virus (TSWV). Populations of tobacco thrips produced on TSWV-infected plants did not differ from those produced on healthy plants, whereas populations varied greatly among host plant species. The mean per plant populations of F. fusca averaged 401, 162, and 10 thrips per plant on Stellaria media, Scleranthus annuus, and Sonchus asper, respectively, during peak abundance in May. Adult F. fusca collected from plant hosts were predominately brachypterous throughout the winter and early spring, but macropterous forms predominated in late spring. Weed hosts varied in their ability to serve as overwintering sources of TSWV inoculum. Following the initial infection by TSWV in October 1997, 75% of Scleranthus annuus and Stellaria media retained infection over the winter and spring season, whereas only 17% of Sonchus asper plants remained infected throughout the same interval. Mortality of TSWV-infected Sonchus asper plants exceeded 25%, but mortality of infected Stellaria media and Scleranthus annuus did not exceed 8%. TSWV transmission by thrips produced on infected plants was greatest on Stellaria media (18%), intermediate on Scleranthus annuus (6%), and lowest on Sonchus asper (2%). Very few viruliferous F. fusca were recovered from soil samples collected below infected wild host plants. Vegetative growth stages of Stellaria media, Sonchus asper, and Ranunculus sardous were more susceptible to F. fusca transmission of TSWV than flowering growth stages, whereas both growth stages of Scleranthus annuus were equally susceptible. In a field study to monitor the spatial and temporal patterns of virus movement from a central source of TSWV-infected Stellaria media to adjacent plots of R. sardous, the incidence of infection in R. sardous plots increased from <1% in March to >42% in June 1999. Infection levels in the Stellaria media inoculum source remained high throughout the experiment, averaging nearly 80% until June 1999 when all Stellaria media plants had senesced. Dispersal of TSWV from the inoculum source extended to the limits of the experimental plot (>37 m). Significant directional patterns of TSWV spread to the R. sardous plots were detected in April and May but not in June. R. sardous infections were detected as early as March and April, suggesting that overwintering inoculum levels in an area can increase rapidly during the spring in susceptible weed hosts prior to planting of susceptible crops. This increase in the abundance of TSWV inoculum sources occurs at a time when vector populations are increasing rapidly. The spread of TSWV among weeds in the spring serves to bridge the period when overwintered inoculum sources decline and susceptible crops are planted.

Life History Traits of Helicoverpa zea (Lepidoptera: Noctuidae) on Non-Bt and Bt Transgenic Corn Hybrids in Eastern North Carolina

Abstract Transgenic varieties of field corn that express the Cry1Ab B. thuringiensis (Bt) toxin in ear tissue present the potential of reducing ear feeding by the corn earworm, Helicoverpa zea (Lepidoptera: Noctuidae), and for reducing the size of populations of the insect infesting other host crops. Life history parameters of H. zea feeding on ears of conventional and Bt field corn varieties were measured in field plots in eastern North Carolina in 1997 and 1998. Transformation events investigated were Mon-810 and Bt-11. Bt corn was found to cause a steady mortality of larvae during development, but permitted ≈15–40% survival to the prepupal stage compared with non-Bt corn. Mortality of prepupae and pupae from Bt corn was also higher than from non-Bt corn, reducing overall adult production by 65–95%. The larvae that did survive grew more slowly on Bt than on non-Bt corn, and produced pupae that weighed 33% less. Pupation and adult eclosion were delayed by 6–10 d by feeding on Bt corn ears. Corn varieties expressing Bt in ear tissue have the potential to reduce H. zea ear feeding by up to 80%, and the potential to reduce populations emerging from ear-stage corn fields to infest cotton, soybean and other crops by around 75%. To have a measurable effect on area-wide populations, Bt corn varieties would need to be planted in large proportions of corn fields. Extensive planting of varieties such as those tested here, having only moderate effects on H. zea, would raise concerns about rapid evolution of resistance.

INTERCROP RELATIONSHIPS AND SPIDER MITE DISPERSAL IN A CORN/PEANUT AGRO‐ECOSYSTEM

Crawling was determined to be an important dispersal mechanism for spider mites leaving border vegetation and entering corn fields early in the season. This dispersal did not appear important in peanut fields. Large populations of spider mites in field corn were found responsible for subsequent infestations in peanuts. As corn plants senesced, mites began crawling to the periphery of the corn plant and grouping in masses on leaf tips, tassels and silks. During this period of mite movement, large numbers of mites were dispersed from the corn on wind currents and carried to nearby host plants. Aerial trapping verified this dispersal of mites and their subsequent colonization of previously uninfested peanut fields. Mites labelled in corn with a fluorescent powder were later found on peanut plants confirming the interhost movement.

2-Undecanone, a constituent of the glandular trichomes of Lycopersicon hirsutum f. glabratum: Effects on Heliothis zea and Manduca sexta growth and survival

The effects of 2‐undecanone, a compound found in the glandular trichomes of the wild tomato, Lycopersicon hirsutum f. glabratum C. H. Mull, PI 134417, on the larvae of Heliothis zea (Boddie) and Manduca sexta (L.) were studied by rearing the larvae on artificial diets containing this chemical. 2‐Undecanone increased larval mortality of H. zea in the first 48 h when combined with 2‐tridecanone, but not alone, and caused deformity and mortality of H. zea pupae both alone and in combination with 2‐tridecanone. 2‐Undecanone had no effect on M. sexta larvae or pupae. Potential implications of these findings for insect pest management are discussed.

Impact of Small Fitness Costs on Pest Adaptation to Crop Varieties with Multiple Toxins: A Heuristic Model

A deterministic two-locus model was used to examine how small fitness costs to individuals carrying resistance alleles could impact the risk of panmictic insect pest populations adapting to crop varieties that produced two distinct toxins. Parameters examined were (1) level of toxicity of each toxin, (2) initial frequencies of alleles for adaptation to the toxins, (3) percentage of population feeding on nontoxic plants, and (4) level of fitness cost associated with adaptation to each of the two toxins. Resistance to each toxin was assumed to be biochemically independent, controlled by a resistance coding allele at a single locus, and inherited as a partially recessive trait in the field. When plants are extremely toxic to the pest, effective refuge size is 10%, and there is a fitness cost to resistance alleles only when in homozygous form (5%), the pest population is never predicted to adapt to either toxin as long as the initial frequencies of the resistance alleles are below 0.05. Even if the initial frequency of the allele for adapting to one toxin is 0.95 when a two-toxin cultivar completely replaces a one-toxin cultivar, the model predicts that a low equilibrium allelic frequency will develop for both resistance alleles, as long as the frequency of the allele for adapting to the second toxin is initially 0.001 or less. If cultivars with one and two toxins are planted, the model predicts that resistance will develop. Nonrandom mating and stochastic variation within subpopulations also could lead to evolution of resistance.

2-tridecanone, tomatoes and Heliothis zea: potential incompatibility of plant antibiosis with insecticidal control

The allelochemic, 2‐tridecanone, which conditions resistance in the wild tomato Lycopersicon hirsutum f. glabratum to Manduca sexta and plays an important role in the resistance to Leptinotarsa decemlineate is shown to induce an enhanced level of tolerance to the carbamate insecticide carbaryl in a third important insect pest of tomato, Heliothis zea. This phenomenon has important implications regarding the compatibility of using tomato cultivars having 2‐tridecanone‐mediated insect resistance in conjunction with insecticides to manage the full spectrum of tomato insect pests.