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Refuge staff estimated that some 20, birds perished this way in Arran Robertson, a spokesman for Oregon Wild, said the Klamath refuges continue to be refuges in name only. In October, refuge managers transferred about 12, acre-feet of water from Tule Lake refuge to Lower Klamath. Austin said the water was put on units containing standing grain from last year, and at the peak, the refuge had about 3, acres of wetlands.

He said right now, water is covering about 2, acres of wetlands. Save my name, email, and website in this browser for the next time I comment. Register Now. During each step or interval, feeding and movement from plant to plant occur. The base movement rate is the proportion that moves from refuge corn, but it is included in calculations for all movement rates. The genotype-specific movement rate is the probability of moving off of Bt corn for each insect genotype. Thus, according to Carroll et al.

They found that mortality due to movement significantly delayed evolution of resistance because of the high rates of movement off of Bt corn. In scenarios with single insecticidal traits, including movement mortality increased Bt corn durability in seed blends relative to fully compliant block refuge. When mortality during movement was included for populations in both blended and block refuge, Onstad also found that increasing this density-independent mortality delayed the evolution of resistance in his model.

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Caprio et al. In their models, the crop only has reproductive tissue and the pest feeds only on this tissue. Thus, the model does not represent pests that feed on vegetative tissue or on other crops. Their results indicated that increasing larval movement rates off of insecticidal kernels tended to increase durability of seed blends. Whether we call this subject farming practices or farmer behavior, the main point is the same: choices made by farmers influence the relative effectiveness of refuge Hurley and Mitchell Some of these choices are directly related to the planting of a refuge, while others pertain to farming practices that can influence the trade-offs between types of refuge.

Separate block refuges should be planted at a recommended level or greater to effectively manage pest resistance. Sometimes the size of a refuge is too small. In other cases, the refuge is planted too far away from the insecticidal crop field. The quality of a separate refuge is influenced by the planting and subsequent management of the crop. If this different quality causes the refuge to be less attractive as a mating site or for oviposition or reduces survival of immature pests, then the block refuge will not contribute as much as intended to resistance management Onstad et al.

The most important and obvious practice that will directly reduce the effectiveness of block refuge is the greater use of insecticides in refuges relative to use in insecticidal crops Onstad et al. Even if the insecticide is not targeted against the primary pest of the insecticidal crop, as long as it is lethal to that pest, it will reduce the effectiveness of the refuge.

Three other farming practices that influence the value of refuge have been the focus of publications: technology adoption, seed saving, and weed management. Adoption of the insecticidal crop in the market is the proportion of the cropland that is planted with an insecticidal crop and its required refuge. Required refuge may be less valuable when adoption is low because a large amount of cropland does not express the insecticidal trait anyway.

Seed saving and weed management can complicate or worsen attempts to manage resistance Krupke et al. For the purposes of this paper and IRM, seed saving means that a farmer collects seed from insecticidal and refuge crops at the end of a growing season and plants them either separately or mixed together in the next season.

Thus, accidental blending may occur. More importantly, the dose of insecticide expressed in the crop may not be consistent in the next season Onstad et al. When seeds of an insecticidal corn crop germinate in the next season and produce weedy or volunteer corn because they are not removed, the weedy corn plants may cause problems for IRM Krupke et al.

The main concern is that lower doses will be expressed in some of the new crop or weeds compared to the expression expected in hybrid insecticidal seed. Here we present two main hypotheses that have been promoted to explain why seed blends may not delay the evolution of resistance as much as a separate block refuge of the same proportional area.

Of course, neither hypothesis by itself allows one to determine whether blends or blocks are better for IRM. A complementary analysis of block refuges is also needed. Fewer formal hypotheses have been promoted to explain why block refuges may not delay the evolution of resistance as much as blended refuge. They postulated that an average refuge plant in a seed blend may not produce as many susceptible insects as the average plant in a block refuge. Feeding during part of the larval stage on insecticidal plants in the seed blend would reduce the survival of susceptible homozygotes and possibly heterozygotes.

Later, a concern for cross-pollination of refuge plants and subsequent reduction in survival due to feeding on insecticidal seed was added to the concerns within this perspective. Survivors from the refuge plants are needed to mate with resistant homozygotes surviving on the insecticidal plants to produce heterozygotes, which are killed by the insecticide. A number of studies have observed reductions in refuge productivity live insects per refuge plant in seed blends compared with blocks of refuge Carroll et al.


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Some have observed no differences Wangila et al. In this view, the most important influence on evolution is the difference in survival between the susceptible homozygotes and the heterozygotes moving to and from refuge and insecticidal plants Brevault et al. Because there are so many processes and factors that determine the production of susceptible homozygotes and heterozygotes in a seed blend Table 1 , it is likely that some cases will be explained by one hypothesis, some will be explained by the other hypothesis, and it is possible that other hypotheses will be postulated in the future.

Furthermore, because these two hypotheses are not mutually exclusive, it is possible that cases will be explained by more than one hypothesis. Here we present three case studies to highlight the types of evaluations that can contribute to decision making. Published case studies for insecticidal corn mostly have concluded that seed blends are satisfactory, whereas most for insecticidal cotton Gossypium hirsutum have drawn the opposite conclusion Heuberger et al.

In Brazil concerns about the high larval movement rates of S. However, still more needs to be learned about this pest. The random mating by O. Onstad and Gould based their model on unpublished and never-described preliminary measurement of larval movement and survival. Davis and Onstad performed a field study to evaluate the Onstad and Gould model and concluded that the amount of plant-to-plant movement and differential survival by O. Several years later, Kang et al. They concluded that for O. Burkness et al. Kang et al. They concluded that because 1 few O. On the basis of all the assumptions described here, they demonstrated that the value of blended refuge is similar to that of block refuge.

Given that mating is non-random in dry, irrigated landscapes described above , blended refuge should be even more valuable for IRM under these conditions. It is not easy to study movement of larvae that are underground. However, Hibbard et al. They concluded that two movement periods were possible during the larval stage.


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  • Onstad analyzed their data to create parameters for his model of the beetle in seed blends, but because of the variability in the observations he did not believe that the data provided clear evidence of secondary movement after the first establishment of the larvae. Therefore, he used the general approach introduced when modeling O. Onstad concluded that seed blends were better than block refuges when all mating occurs in the natal field.

    In —, Murphy et al. In —, Zukoff et al. Pan et al. They used the single-movement model for larvae Onstad but changed the values of two parameters based on the data of Binning et al. They also calculated a probability of movement away from insecticidal corn slightly greater than that for refuge corn. Because adults do not fly very far before mating Spencer et al. Because of this non-random mating and less than full compliance by farmers in planting block refuge, modeling results indicated that the seed-blend scenarios in many cases produced equal or greater durability than block refuges that were relocated each year Pan et al.

    Thus, for D. This conclusion was also supported by an economic analysis of D. Because the larvae of H. First, we need to understand how frequently this pest feeds on the various tissues on corn ears. Horner et al. They stated on page ,Furthermore, exposure to the expressed toxin may be related to the condition of silk tissue at the time of egg hatch. Larvae hatching from eggs laid on wilted or brown silks may have a greater chance of surviving intoxication episodes because of reduced toxin expression in the senescent tissue.

    Plant stress may also contribute to the varied responses among locations. The NC site, which showed the lowest Bt-induced effects, was not irrigated, and thus rapid dry-down of silk tissue and possible acceleration of kernel maturation may have lowered toxin expression.

    Thus, commonly observed silk feeding can increase survival on cross-pollinated corn ears. Feeding on the ear tip also provides less or non-toxic maternal tissue for the larvae. Kernel area consumed varied much more from site to site and year to year than within replicates Horner et al. To understand the impact of cross-pollination on H.

    During the reproductive stage of corn, H.

    Blended Refuge and Insect Resistance Management for Insecticidal Corn

    The refuge ear is composed of fertilized kernels and maternal tissues husk, silk, shank, and cob. Only kernels originating from cross-pollination will express insecticidal traits. It is not uncommon to find H. Bioassays with H. As a consequence, it is likely that H. Development of H. It is also possible that a larva could avoid lethal exposure by feeding exclusively on maternal tissue in the ear tip or feeding only on kernels that do not express Bt proteins Horner et al.

    The pattern of kernel damage caused by intoxicated H. Therefore, the survival by H. For H. We believe that the effects of cross-pollination and our ability to observe these effects are likely influenced by many factors including weather, corn hybrid, cultivation practices, H. Furthermore, the susceptibility of H. For a long-term study of resistance evolution, the mean effect will likely give us a reasonable understanding of consequences for evolution and IRM.

    In the southern United States, cross-pollination affects larvae only in the second generation on corn and only in one of the four generations per year selected by insecticidal traits two on corn, two on cotton. Summary of replicated field studies measuring survival of H. Table 3 summarizes the published field trials concerning survival in cross-pollinated blended refuges.

    Yang et al. It is not clear what effect starting the neonates on significantly manipulated corn ears had on feeding behavior. When all 14 field trials are considered, the mean survival is 0. Note that 6 out of 14 trials had survival of 1 indicating at least as many larvae surviving on cross-pollinated refuge corn as on the pure refuge. When we separated results by insecticidal trait or type of infestation, no clear patterns were identified Table 3.

    In the model, H. Using Figure 3 of Pan et al. Durability is estimated to be from 18 to 23 yr depending on the amount of blended corn refuge. Mallet and Porter concluded that as IRM researchers investigate real systems, it is likely that the IRM plan will be situation dependent. This conclusion that the use of blended refuge should be considered on a case-by-case basis is supported by others Onstad et al. As this review has indicated, farmer behavior must also be considered on a case-by-case basis before developing a refuge strategy.

    Even if we cannot a priori determine which pests should be managed with one kind of refuge, can we identify any real systems for which seed blends are not likely to be helpful? If a crop canopy has significant overlap of stems and leaves from adjacent plants, it is likely that pests would feed on both refuge and insecticidal plants. Unless we believe that a pest can constantly monitor its food and sense its substrate and move to refuge as necessary, it is not likely that these crops would provide the right environment for blended refuge.

    If farmers are unlikely to grow a separate block refuge for economic or cultural reasons, then blended refuge may be the only choice unless significant unstructured, natural refuge exists in the landscape. As Head and Savinelli indicated, the local cultural and agronomic conditions must be considered when developing an IRM strategy.

    The decision to pyramid multiple insecticidal traits is not exempt from the complexities highlighted in our review. Under ideal conditions, pyramids can delay the evolution of resistance relative to the use of single traits. But with regard to refuge deployment and configuration, we believe that pyramids are not unique. They should be evaluated for impact on genotypic survival just like any single insecticidal trait.

    Then this information should be combined with other knowledge of pest biology and farming practices to make a decision Carroll et al. Data on behavior of adult or immature insects cannot be collected inexpensively. Researchers need to remain persistent and dedicated to understanding nature. Given the complexity of the factors influencing the trade-off between blended refuge and separate block refuges, it is likely that modeling will continue to play a key role in the evaluation of refuge strategies.

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    National Center for Biotechnology Information , U. Environ Entomol. Published online Dec 4. Author information Article notes Copyright and License information Disclaimer. Corresponding author, e-mail: moc. Received Jun 9. For commercial re-use, please contact journals. Abstract In this review, we evaluate the intentional mixing or blending of insecticidal seed with refuge seed for managing resistance by insects to insecticidal corn Zea mays. Keywords: IPM, seed mixture, seed blend, Bt corn, refuge. Table 1. What is survival of genotype after leaving Bt plant and arriving on refuge?

    What is survival of genotype after leaving refuge and arriving on Bt plant? What is survival of genotype due to movement? What is probability of leaving insecticidal plant? What is probability of leaving refuge plant? What are movement rates at various pest densities? How many moves from plant to plant with feeding in between? What is the timing of movement s relative to age of larva? Does first movement occur without feeding first? Are there differences in movement for insect genotypes? What is probability of feeding on fertilized plant tissue after pollination?

    What is survival of genotype on fertilized plant tissue? How does cross-pollination with insecticidal trait affect survival in refuge? Are there differences in any parameter due to growth stage of crop? Open in a separate window.

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    Table 2. Do females or males mate before dispersing out of natal field? What is proportion of each gender that mates before dispersing? Can each gender mate more than once? Over how many days can each gender mate more than once? How far can a male or female disperse before mating? How does pest density influence behavior? Does the female oviposit mostly in natal field? Are there differences in adult dispersal for insect genotypes? Are there differences in emergence for insect genotypes?

    Does adult emergence and behavior differ in the refuge and insecticidal fields? Are there differences in any parameter due to growth stage s of crop s? Survival Survival is the most important biological parameter to understand the impacts of seed blends for IRM including survival before and after movement, on vegetative and reproductive tissues, and during movement Table 1. Larval Movement We need to understand movement from plant to plant, and sometimes, within a plant. Adult Behavior To appreciate the value of seed blends relative to separate block refuges, we need to know several aspects of adult behavior Table 2.

    Separate Block Refuge Modeling has shown that a well-positioned block refuge is most effective when it remains in the same location year after year and the males disperse widely for random mating while females remain in natal refuge to mate and lay eggs Guse et al. Comparison of Models Mallet and Porter and Tabashnik used abstract models of an insect population under selection by an insecticidal crop to explore the value of seed blends versus separate block refuges. Farmer Behavior Whether we call this subject farming practices or farmer behavior, the main point is the same: choices made by farmers influence the relative effectiveness of refuge Hurley and Mitchell Hypotheses Here we present two main hypotheses that have been promoted to explain why seed blends may not delay the evolution of resistance as much as a separate block refuge of the same proportional area.

    Case Studies Regarding Insecticidal Corn Here we present three case studies to highlight the types of evaluations that can contribute to decision making. Survival of H. Table 3. Synthesis of Knowledge about H. Conclusions Mallet and Porter concluded that as IRM researchers investigate real systems, it is likely that the IRM plan will be situation dependent. Acknowledgments We thank April Battani and three reviewers for helping improve the manuscript. References Cited Ali A. Activity of Bacillus thuringiensis Berliner against different ages and stages Helicoverpa zea Lepidoptera: Noctuidae on cotton.

    Corn earworm Lepidoptera: Noctuidae biology on food corn on the high plains. Implications of volunteer corn and cross-pollination of Bt and non-Bt corn on corn earworm Lepidoptera: Noctuidae Bt resistance management. The European corn borer, Pyrausta nubilalis Hubn. Larval movements of Chilo partellus Lepidoptera: Pyralidae within and between plants: timing, density responses and survival. Double fertilization — caught in the act. Trends Plant Sci. Estimating western corn rootworm Coleoptera: Chrysomelidae larval susceptibility to event DAS—7 maize. A seed mixture increases dominance of resistance to Bt cotton in Helicoverpa z ea.

    Scientific Rep. Cross-pollination of nontransgenic corn ears with transgenic Bt corn: efficacy against Lepidopteran pests and implications for resistance management. Bt maize seed mixtures for Helicoverpa zea Lepidoptera: Noctuidae : larval movement, development, and survival on non-transgenic maize. Corn Earworm.

    Accessed 14 September Caprio M. The impact of inter-kernel movement in the evolution of resistance to dual-toxin bt-corn varieties in Helicoverpa zea Lepidoptera: Noctuidae. Can pyramids and seed mixtures delay resistance to Bt crops? Trends Biotechnol. Resistance management for sustainable use of Bacillus thuringiensis crops in integrated pest management.

    In Horowitz A. Insect pest management. Springer, Heidelberg, Germany. When and where a seed mix refuge makes sense for managing insect resistance to Bt plants. Crop Prot. Theoretical and empirical assessment of a seed mix refuge in corn for southwestern corn borer. The development of insecticide resistance in the presence of migration. Survival of corn earworm Lepidoptera: Noctuidae on Bt maize and cross-pollinated refuge ears from seed blends. On-plant survival and inheritance of resistance to Cry1Ab toxin from Bacillus thuringiensis in a field-derived strain of European corn borer, Ostrinia nubilalis.

    Pest Manag. Fitness costs of Cry1Ab resistance in a field-derived strain of Ostrinia nubilalis Lepidoptera: Crambidae. Resistance evolution to Bt crops: predispersal mating of European corn borers. PLoS Biology 4 : — European corn borer Lepidoptera: Pyralidae feeding behavior and survival on transgenic corn containing Cry1A b protein from Bacillus thuringiensis. Seed mixtures as a resistance management strategy for European corn borers Lepidoptera: Crambidae infesting transgenic corn expressing Cry1Ab protein.

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    Evidence for obligate migratory flight behavior in young European corn borer Lepidoptera: Crambidae females. Movement and survival of Busseola fusca Lepidoptera: Noctuidae larvae within maize plantings with different ratios of non-Bt and Bt seed. Genetic and biological influences in the evolution of insecticide resistance. Dispersal and movement behavior of neonate European corn borer Lepidoptera: Crambidae on non-Bt and transgenic Bt corn.

    Selective feeding of tobacco budworm and bollworm Lepidoptera: Noctuidae on meridic diet with different concentrations of Bacillus thuringiensis proteins. Arthropod behavior and the efficacy of plant protectants.

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    Potential and problems with high-dose strategies for pesticidal engineered crops. Biocontrol Sci. Moving beyond resistance management toward an expanded role for seed mixtures in agriculture. Modeling the development of resistance by stalk-boring Lepidoptera Crambidae in areas with irrigated, transgenic corn. Chilo partellus in maize: neonate behavior, field dispersal and infestation. Indian J.