Progress 09/01/08 to 08/31/12
Outputs
OUTPUTS: The commercialization of plants expressing insecticidal crystal (Cry) proteins from Bacillus thuringiensis (Bt) for insect management has revolutionized agriculture and become a major tool for integrated pest management (IPM) programs. In 2011, Bt crops were grown on more than 66 million ha in 26 countries. Bt crops have provided economic benefits to growers and reduced the use of other insecticides, suppressed pest populations on a regional basis, conserved natural enemies and promoted biological control services in agricultural landscapes. However, the evolution of insect resistance is a major threat to the sustainable use of Bt crops. Resistance to Bt plants is a serious concern, but there are only four clear cases. Commonly proposed reasons for the few confirmed cases of resistance to Bt plants are the high dose of Bt proteins expressed in plants and the use of refuges of non-Bt plants that can serve as a pool of Bt susceptible alleles in the population. Another possible reason for the relatively few cases of resistance to Bt plants could be their safety to natural enemies that help suppress pest populations. Numerous studies have investigated the effects of Bt crops and Cry proteins on natural enemies (predators and parasitoids) in the laboratory and field. In total, these studies have confirmed the safety of Bt proteins, especially when compared to traditional insecticides. The conservation of natural enemies by the use of Bt plants could also influence evolution of resistance to Bt crops. This question was first studied by Gould et al. in their conceptual and mathematical models on tritrophic interactions of a plant, an herbivore and a natural enemy. Their simplest conclusion was that natural enemies which increase differential fitness between susceptible and resistant phenotypes on host plants will accelerate evolution of resistance; those that decrease the differential will delay resistance. The literature contains suggestions that natural enemies could delay or accelerate resistance, depending whether there is a differential impact on susceptible or resistant phenotypes. While these examples are useful, they have not been tested over multiple generations using a Bt crop, an insect pest that has evolved resistance to a Bt protein expressed in the crop, and a natural enemy. Thus, our studies are the first that directly addresses the role of a natural enemy influencing the evolution of resistance to a Bt crop. Our objectives were to determine: if a natural enemy can delay the evolution of insect resistance to a Bt crop, and: if biological control in conjunction with Bt crops can effectively suppress the pest population. In addition, to design field-realistic conditions for both the predator and prey, we sprayed refuges in some treatments and observed those effects on the evolution of insect resistance. The results of our studies have been disseminated to the agricultural, scientific and regulatory community through five publications and numerous scientific talks. PARTICIPANTS: The individuals who worked on the grant are reflected in the publications. XX Liu and M Chen performed much of the work while visiting scientists in the Shelton program. Both came from Chinese universities and Liu returned while Chen was hired at Monsanto. D Onstad from Illinois and R. Roush helped with project design and data analysis and H Collins assisted Chen and Liu. TARGET AUDIENCES: The target audiences were agricultural scientists, farmers and the regulatory community. The results have been disseminated to them in publications and numerous scientific talks. PROJECT MODIFICATIONS: Part 3 (field studies) of the original project could not be performed because of inclement weather.
Impacts
We used a model system composed of Bt broccoli expressing Cry1Ac, a population of the pest Plutella xylostella carrying a low percentage of alleles resistant to Cry1Ac and the insecticide spinosad, and a natural enemy, Coleomegilla maculata, to conduct an experiment over multiple generations. The results demonstrated that P. xylostella populations were very low in the treatment containing C. maculata and unsprayed non-Bt refuge plants after 6 generations. Furthermore, the evolution of resistance to Bt plants was significantly slower in this treatment. In contrast, Bt plants were completely defoliated and control failures were observed in treatments without C. maculata after 4-5 generations. In the treatment containing sprayed non-Bt refuge plants and C. maculata, the P. xylostella population was low although the speed of resistance selection to Cry1Ac was significantly increased. While farmers are concerned with reducing the likelihood of resistance, they are more immediately concerned with lowering the pest population to avoid crop injury. It is well worth noting that in our experiments we not only saw the lowest rate of resistance evolution in the prey when the predator was not decimated by the use of an insecticide, but also the lowest and least fluctuating pest population on the Bt plants and low and stable pest populations on the non-Bt plants in the refuge. Thus, it is evident from our experiments that farmers can have the best of both worlds if they combine Bt plants with biological control. We suggest that host-plant resistance with Bt plants and biological control can be fully compatible within an overall integrated pest management (IPM) program. Our results have significant implications for IPM and insect resistance management (IRM) for Bt crops.
Publications
- Liu, X. X., M. Chen, H.L. Collins, D. W. Onstd, R. T. Roush, Q. Zhang, E. D. Earle and A.M. Shelton. 2013. Natural enemies delay insect resistance to transgenic insecticidal crops. PNAS (in review)
- Onstad, D., X. Liu, M. Chen, R. Roush and A. M. Shelton. 2013. Modeling the integration of parasitism, insecticide and transgenic insecticidal crops for the long-term control of an insect pest. J. Econ. Entomol. (in press).
- Liu, X., M. Chen, D. Onstad, R. Roush, H. Collins, E. D. Earle and A. M. Shelton. 2012. Effect of Bt broccoli or broccoli treated with insecticides on ovipositional preference and larval survival of Plutella xylostella (Lepidoptera: Plutellidae). Environ. Entomol. 41: 880-886.
- Liu, X., M. Chen, H. Collins, D. Onstad, R. Roush, Q. Zhang and A. M. Shelton. 2012. Effect of insecticides and Plutella xylostella genotype on a predator and parasitoid and implications for the evolution of insecticide resistance. J. Econ. Entomol. 105: 354-362.
- Liu, X., M. Chen, D. Onstad, R. Roush and A. M. Shelton. 2011. Effects of Bt broccoli and resistant genotypes of Plutella xylostella on development and host acceptance of the parasitoid, Diadegma insulare. Transgenic Research Vol 20: 887-897. DOI 10.1007/s11248-010-9471-9
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Progress 09/01/10 to 08/31/11
Outputs
OUTPUTS: The effects of broccoli type (normal or expressing Cry1Ac protein) and insect genotype (susceptible or Cry1Ac-resistant) of Plutella xylostella L. (Lepidoptera: Plutellidae) were examined for their effects on the development and host foraging behavior of the parasitoid, Diadegma insulare (Cresson) (Hymenoptera: Ichneumonidae) over two generations. Parasitism rate and development of D. insulare were not significantly different when different genotypes (Bt-resistant or susceptible) of insect host larvae fed on non-Bt broccoli plants. D. insulare could not discriminate between resistant and susceptible genotypes of P. xylostella, nor between Bt and normal broccoli plants with different genotypes of P. xylostella feeding on them. No D. insulare could emerge from Bt broccoli-fed susceptible and heterozygous P. xylostella larvae because these larvae were unable to survive on Bt broccoli. The parasitism rate, developmental period, pupal and adult weights of D. insulare that had developed on Bt broccoli-fed Cry1Ac-resistant P. xylostella larvae were not significantly different from those that developed on non-Bt broccoli-fed larvae. Female D. insulare emerged from Cry1Ac-resistant P. xylostella that fed on Bt plants could successfully parasitize P. xylostella larvae. The life parameters of the subsequent generation of D. insulare from P. xylostella reared on Bt broccoli were not significantly different from those from non-Bt broccoli. The Cry1Ac protein was detected in P. xylostella and in D. insulare when hosts fed on Bt broccoli. These results are the first to indicate that Cry1Ac did not harm the development or host acceptance of an important endoparasitoid after two generations of exposure. The ovipositional preference of strains (RR, RS, SS) of P. xylostella resistant to Cry1Ac-expressing broccoli or broccoli treated with lambda-cyhalothrin or spinosad were studied. Numbers of eggs per plant did not differ between Bt broccoli and non-Bt broccoli for RR, RS and SS adults. Adults also could not discriminate between spinosad-treated and untreated plants, and oviposition did not increase over the 13 days after spinosad treatment. For broccoli treated with lambda-cyhalothrin at the diagnostic dose of 20 ppm, all three insect strains had constant oviposition over time based on linear regressions. At the field dose of 80 ppm, the RR strain had constant oviposition over time. The SS susceptible strain had increasing oviposition over time, but the oviposition pattern on the non-sprayed broccoli also increased over time. Susceptible females oviposited fewer eggs on plants sprayed with lambda-cyhalothrin than on unsprayed plants. A residue-persistence test showed that spinosad and lambda-cyhalothrin could effectively control SS P. xylostella larvae for 7-9 days after application. These results will provide data needed for our model on the effect of natural enemies on the evolution of resistance to Bt plants and conventional insecticides. PARTICIPANTS: Xiaoxia Liu from Chinese Academy of Sciences David Onstad from the University of Illinois Rick Roush from the University of Melbourne Mao Chen from Monsanto TARGET AUDIENCES: The target audience are regulators of biotech products and the scientific community who works on insect resistant GM crops. PROJECT MODIFICATIONS: None
Impacts
These results will provide data needed for our model on the effect of natural enemies on the evolution of resistance to Bt plants and conventional insecticides.
Publications
- Liu, X., M. Chen, D. Onstad, R. Roush, H. Collins and A. M. Shelton. 2012. Effect of Bt broccoli or broccoli treated with insecticides on ovipositional preference of Plutella xylostella (Lepidoptera: Plutellidae). Environ. Entomol.(in press)
- Liu, X., M. Chen, D. Onstad, R. Roush and A. M. Shelton. 2011. Effects of Bt broccoli and resistant genotypes of Plutella xylostella on development and host acceptance of the parasitoid, Diadegma insulare. Transgenic Research Vol 20: 887-897. DOI 10.1007/s11248-010-9471-9.
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Progress 09/01/09 to 08/31/10
Outputs
OUTPUTS: The goal of this project is to make a comparative assessment of the effects of Bt plants and conventional insecticides on the persistence and population dynamics of a parasitoid and predator and, in turn, their effects on pest suppression and evolution of insecticide resistance in the pest population. To accomplish this we will use our unique tritrophic system of insects that carry resistance to a Bt toxin and two different conventional insecticides, plants that express the Bt toxin, and natural enemies that are suitable for the test. Our studies comprise a set of laboratory, greenhouse, field, and modeling experiments that will help create an understanding of this tritrophic system. We will also explore a general version of the model to provide insights into the dynamics of a broader range of tritrophic systems. The information from our studies will help develop scientifically-based decisions about the effects of introducing GM insect-resistant plants into the environment compared to conventional technologies. The outcome of our work will help regulators make more informed decision and help producers develop programs with enhanced biological control and insect resistance management (IRM) components within the context of overall IPM programs. PARTICIPANTS: Participants who worked on the research part of the project from the Entomology Department at Geneva are Dr. M. Chen, Dr. Xiaoxia Liu and Dr. A. M. Shelton. Dr. David Onstad from the Department of Environmental Biology at the University of Illinois is working on the modeling part of the proposal. TARGET AUDIENCES: The target audiences are government policy makers, companies that sell Bt transgenic plants and scientists interested in insecticide resistance management programs. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
The long-term goal of our project is to provide scientifically-based information to regulatory agencies on the environmental effects of Bt plants compared to conventional insecticides. Specifically, we wish to increase our understanding of the effects of Bt plants and conventional insecticides on the persistence and population dynamics of natural enemy populations and how these may affect the rate of evolution of resistance to Bt plants and insecticides in their host. As a first step in examining we used a unique system of resistant insects, Bt plants and a parasitoid. The effects of broccoli type (normal or expressing Cry1Ac protein) and insect genotype (susceptible or Cry1Ac-resistant) of Plutella xylostella L. (Lepidoptera: Plutellidae) were examined for their effects on the development and host foraging behavior of the parasitoid, Diadegma insulare (Cresson) (Hymenoptera: Ichneumonidae) over two generations. Parasitism rate and development of D. insulare were not significantly different when different genotypes (Bt-resistant or susceptible) of insect host larvae fed on non-Bt broccoli plants. D. insulare could not discriminate between resistant and susceptible genotypes of P. xylostella, nor between Bt and normal broccoli plants with different genotypes of P. xylostella feeding on them. No D. insulare could emerge from Bt broccoli-fed susceptible and heterozygous P. xylostella larvae because these larvae were unable to survive on Bt broccoli. The parasitism rate, developmental period, pupal and adult weights of D. insulare that had developed on Bt broccoli-fed Cry1Ac-resistant P. xylostella larvae were not significantly different from those that developed on non-Bt broccoli-fed larvae. Female D. insulare emerged from Cry1Ac-resistant P. xylostella that fed on Bt plants could successfully parasitize P. xylostella larvae. The life parameters of the subsequent generation of D. insulare from P. xylostella reared on Bt broccoli were not significantly different from those from non-Bt broccoli. The Cry1Ac protein was detected in P. xylostella and in D. insulare when hosts fed on Bt broccoli. These results are the first to indicate that Cry1Ac did not harm the development or host acceptance of an important endoparasitoid after two generations of exposure. We are building on this work with long term cage studies to examine the effect of biological control agents on resistance evolution.
Publications
- Liu, X., M. Chen, D. Onstad, R. Roush and A. M. Shelton. 2010. Effects of Bt broccoli and resistant genotypes of Plutella xylostella on development and host acceptance of the parasitoid, Diadegma insulare. Transgenic Research (in press)
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Progress 09/01/08 to 08/31/09
Outputs
OUTPUTS: Prior to the large cage tests beginning, a series of laboratory experiments were conducted. They have demonstrated: 1) Plutella xylostella adults could not discriminate between Bt broccoli or plants treated with lambda-cyhalothrin or spinosad; 2) Bt broccoli is safer to the parasitoid Diadegma insulare and the predator Coleomagilla maculata than either lambda-cyhalothrin or spinosad. In addition, we are in the middle of running cage experiments to determine the impact of Bt broccoli, lambda-cyhalothrin and spinosad on the population dynamics and resistance evolution in Plutella xylostella. PARTICIPANTS: Participants who worked on the research part of the project from the Entomology Department at Geneva are Dr. M. Chen, Dr. Xiaoxia Liu and Dr. A. M. Shelton. Dr. David Onstad from the Department of Environmental Biology at the University of Illinois is working on the modeling part of the proposal. TARGET AUDIENCES: The target audiences are government policy makers, companies that sell Bt transgenic plants and scientists interested in insecticide resistance management programs. PROJECT MODIFICATIONS: We have found that the predators and parasitoids are very effective in reducing the pest populations when Bt plants are used, compared to lambda-cyhalothrin and spinosad. Hence, we are now emphasizing their role in an overall IPM program and giving less emphasis to their influence on insecticide resistance management. However, resistance allele frequency will continue to be documented.
Impacts
The impact of our findings will only be known upon completion of the project.
Publications
- No publications reported this period
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