Modeling the integration of parasitoid, insecticide, and transgenic insecticidal crop for the long-term control of an insect pest.

The tools of insect pest management include host plant resistance, biological control, and insecticides and how they are integrated will influence the durability of each. We created a detailed model of the population dynamics and population genetics of the diamondback moth, Plutella xylostella L., and its parasitoid, Diadegma insulare (Cresson), to study long-term pest management in broccoli Brassica oleracea L. Given this pest's history of evolving resistance to various toxins, we also evaluated the evolution of resistance to transgenic insecticidal Bt broccoli (expressing Cry1Ac) and two types of insecticides. Simulations demonstrated that parasitism provided the most reliable, long-term control of P. xylostella populations. Use of Bt broccoli with a 10% insecticide-free refuge did not reduce the long-term contribution of parasitism to pest control. Small refuges within Bt broccoli fields can delay evolution of resistance > 30 generations if resistance alleles are rare in the pest population. However, the effectiveness of these refuges can be compromised by insecticide use. Rainfall mortality during the pest's egg and neonate stages significantly influences pest control but especially resistance management. Our model results support the idea that Bt crops and biological control can be integrated in integrated pest management and actually synergistically support each other. However, the planting and maintenance of toxin-free refuges are critical to this integration.

Effect of insecticides and Plutella xylostella (Lepidoptera: Plutellidae) genotype on a predator and parasitoid and implications for the evolution of insecticide resistance.

In the laboratory and in cages in the greenhouse, we evaluated the toxicity of two insecticides (lambda-cyhalothrin and spinosad) on the parasitoid, Diadegma insulare (Cresson), and the predator, Coleomegilla maculate (DeGeer), both natural enemies of the diamondback moth, Plutella xylostella (L.). Lambda-cyhalothrin was very toxic to both natural enemies. Spinosad was less toxic to C. maculata adults and larvae, and slightly toxic to D. insulare. Both natural enemies suppressed P. xylostella populations in cages with 80% spinosad-treated and 20% nontreated plants; such suppression was not seen when lambda-cyhalothrin was used. Using broccoli, Brassica oleracea L. variety italica, a common host for P. xylostella, we also studied direct and indirect effects of both natural enemies in the presence and absence of the two insecticides and to different P. xylostella genotypes: resistant to the insecticide, susceptible, or heterozygous. Neither natural enemy could distinguish host genotype if P. xylostella were feeding on nontreated plants. They could also not distinguish between larvae feeding on spinosad-treated plants and nontreated plants, but D. insulare could distinguish between larvae feeding on lambda-cyhalothrin treated and nontreated plants. Our studies suggest that lambda-cyhalothrin has direct toxicity to these two natural enemies, can affect their host foraging and acceptance of P. xylostella and consequently would not be compatible in conserving these natural enemies in a program for suppression of P. xylostella. In contrast, our studies suggest that treatment with spinosad has much less effect on these natural enemies and would allow them to help suppress populations of P. xylostella. These findings are discussed in relation to the evolution of insecticide resistance and suppression of the pest populations.

Developmental penalties associated with inducible tolerance in Helicoverpa armigera to insecticidal toxins from Bacillus thuringiensis.

Exposure of insect larvae to sublethal concentrations of crystal toxins from the soil bacterium Bacillus thuringiensis (Bt toxins) causes the induction of immune and metabolic responses that can be transmitted to offspring by epigenetic inheritance mechanisms. Given that the elevated immune status carries significant developmental penalties, we wanted to establish the relationships between immune induction, tolerance to the toxin and developmental penalties. A laboratory culture of Helicoverpa armigera was induced by a sublethal bacterial suspension containing crystal toxin Cry1Ac in one generation and maintained in the presence of toxin, acquiring significant levels of tolerance to the toxin within 12 generations of continuous exposure. Comparing tolerant and susceptible insects, we show that the induction of larval immune response and the coincident alteration of development-related metabolic activities by elicitors in the larval gut (larval induction) differs from the elevated immune status transmitted by epigenetic mechanisms (embryonic induction). Because the damaging effects of larval induction processes are higher compared to embryonic induction, it is likely that overall developmental penalties depend on the relative contribution of the two induction processes. When insects are kept with the same amount of toxin in the diet for subsequent generations, the embryonic induction process increases its contribution compared to the larval induction, resulting in reduced overall developmental penalty, while tolerance to the toxin is maintained.

Effect of Bt broccoli and resistant genotype of Plutella xylostella (Lepidoptera: Plutellidae) on development and host acceptance of the parasitoid Diadegma insulare (Hymenoptera: Ichneumonidae).

The ecological implications on biological control of insecticidal transgenic plants, which produce crystal (Cry) proteins from the soil bacterium Bacillus thuringiensis (Bt), remain a contentious issue and affect risk assessment decisions. In this study, we used a unique system of resistant insects, Bt plants and a parasitoid to critically evaluate this issue. 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 suggest that using other Bt crops and resistant insect species would likely lead to similar conclusions about the safety of the presently used Bt proteins on parasitoids.