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Pesticide Resistance: Strategies and Tactics for Management. 1986. National Academy Press, Washington, D.C. Preventing or Managing Resistance in Arthropods JOHN R. BEEPER, RICHARD T. ROUSH, and HAROLD T. REYNOLDS Insecticide resistance is a widespread problem for which man- agement tactics have been developed but have not been put into widespread practice. Genetic, reproductive, behaviorallecological, and agronomiclcontrolfactors over which we have varying degrees of control influence the rate of resistance development and are key to its management. Resistance management tactics should be aimed at reducing allele frequencies, reducing dominance, and minimizing the fitness of resistance genotypes. Adequate information to confi- dently choose which of these tactics to use is lacking and prevents their practical use. Basic resistance research in genetics, biochem- istry, physiology, and toxicology on agronomic pests is needed. The discriminate use of insecticides needs to be strengthened within in- tegrated pest management. Improved monitoring techniques that al- low for the detection of resistance at low frequencies within populations are needed. INTRODUCTION Many resistance management tactics have been identified over the past 40 years, but few have been put into practice; of those, most are being used to improve crop production rather than to manage resistance (e.g., economic thresholds rather than calendar spray schedules). Another problem in man- aging pesticide resistance is that each interest group (e.g., pesticide manu- facturers, regulators, researchers, extension personnel, farmers, and public health workers, and the consumer) has a different perspective on the problem 335
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336 TACTICS FOR PREVENTION AND MANAGEMENT and on how it should be solved. These scientific, economic, and social/ political constraints increase the complexity of the problem, because not only must we develop scientific answers to the resistance problem, we must also develop answers that meet the needs of the different interest groups. RATE DETERMINING FACTORS Resistance develops at different rates between species and even between populations of the same species due to genetic, reproductive, behavioral/ ecological, and operational factors (Georghiou and Taylor, 1977a,b; Geor- ghiou, 1980a,b, 1983; Wood and Bishop, 19811. The general consensus is that only the operational factors can be manipulated-everything else is beyond our control (Wood and Bishop, 1981; Georghiou, 19831. The only limitation to what is "operational," however, may be our ability to recognize how to manipulate it. For example, migration in and out of treated habitats is generally assumed to be a biological factor beyond our control. Croft and colleagues, however, have been experimenting with techniques such as pher- omone lures to reintroduce susceptible genes into the treated habitats (Croft, 19841. Also, dominance of resistance was considered a genetic, nonopera- tional factor until Curtis et al. (1978) introduced the concept that dominance might be modified by the insecticide dose applied (effective dominance). Directly changing pest biologies holds promise for indirectly manipulating resistance development. For example, the Heliothis complex, including He- liothis zea (Boddie) and H. virescens (F.), are among the most chronic, difficult to control pests in North American cotton. H. virescens is particularly troublesome because it has developed resistance to every major insecticide class (Sparks, 1981; Martinez-Carrillo and Reynolds, 19831. An alternative to chemical control, which can be considered an indirect resistance man- agement tactic, is the Heliothis backcross hybrid (Proshold et al., 19831. Crosses of H. virescens with H. suLflexa (Guenee) produce fertile daughters and sterile sons (Laster, 1972), which is perpetuated through successive generations and can reduce the rate of population increase. Spider mites (Tetranychus spp.) are pests of many orchard and field crops throughout the world. Cotton seedlings can be induced to produce substances, through infestation with mites, that dramatically retard mite population growth on reinfestation (Karban and Carey, 19841. These substances also can be transported systemically within the plants and will have some degree of residual activity (up to 12 days). Although it may be some time before it is practical to inoculate cotton plants with mites to prevent mite outbreaks in the field, more immediate practical benefits from this research are possible. Plant breeders and genetic engineers could develop plant varieties with el- evated intrinsic levels of the responsible substances. Or chemicals could be
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RESISTANCE IN ARTHROPODS 337 developed that, when applied to crops, would induce production of plant chemicals. Influencing the reproductive rate of arthropods also offers potential for resistance management. Reducing the number of offspring per generation or the number of generations per year may reduce the need for insecticide applications. Although these tactics have not been held in high regard, be- cause they have not been effective enough to replace pesticides, they could be used together with other pest-management practices. These examples illustrate that some genetic, reproductive, and behavioral/ ecological factors have operational components. Therefore, the term "ag- ronomic/control" should be substituted for "operational." Agronomic refers to the various cultural practices in cropping systems, while control refers to the control and management practices in both agricultural and medical/vet- erinary situations. This change in terminology (1) more clearly defines the factors, (2) opens areas for consideration not traditionally thought to be within our control, and (3) encourages the further development of novel tactics less directly related to insecticide use. TACTICS The tactics thus far developed to prevent or manage insecticide resistance have tended to be directly related to insecticide use, which is expected, since primarily toxicologists and entomologists have addressed the problem. In- secticides, however, are only one part of resistance development. For ex- ample, the rate of change in allele frequency at any given locus in a closed population is a function of initial allele frequency, dominance, and the relative fitness of the various genotypes (Futuyma, 1979~. Resistance develops more rapidly with dominance, higher gene frequencies, and a greater fitness ad- vantage to resistant genotypes (Georghiou and Taylor, 1977a). One objective of resistance management is to maintain resistance alleles at very low fre- quencies. Thus, resistance management tactics should be aimed at reducing allele frequencies, reducing dominance, and minimizing the fitness of resis- tant genotypes. Reducing Frequencies of Resistant Alleles A commonly suggested method for directly reducing resistance allele fre- quencies is by diluting them through the mass release of susceptible insects, for example, the mass release of susceptible male mosquitoes to dilute re- sistance (Curtis et al., 19781. This tactic has not been put to practical field use, partly because of the cost of such a program. Another suggested method has been to eradicate resistance foci. Stringent quarantine measures and alternative controls could be used to eliminate newly established resistant
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338 TACTICS FOR PREVENTION AND MANAGEMENT foci (Sutherst and Comins, 1979). This approach requires extensive quar- antine procedures and improved detection capabilities. Decreasing Dominance of Resistance High insecticide use rates can change the effective dominance of resistance (Curtis et al., 19781; rates that kill heterozygotes can make resistance effec- tively recessive. Immigration of susceptible individuals and low-resistance gene frequencies is very important to this approach (Tabashnik and Croft, 1982~. The rates required to kill heterozygotes, however, might not be eco- nomically practical and might not be identified until after the heterozygotes achieve a high frequency within a population. Minimizing Fitness of Resistant Genotypes Most resistance management tactics involve reducing fitnesses of resistant genotypes relative to susceptible genotypes by either preserving susceptible homozygotes or eliminating heterozygotes and resistant homozygotes. Fitness can be lowered by reducing insecticide use rates, extending intervals between treatments, using short residual insecticides, and the like. Determining which tactic is most appropriate and will maintain effective control, however, is difficult. Susceptible homozygotes can be preserved by creating refugia where part of the population is not treated (Georghiou and Taylor, 1977b). Pres- ervation may be achieved by (1) leaving areas unsprayed, (2) using higher action thresholds that tend to reduce the number of insecticide applications, (3) applying short residual compounds that reduce the effective exposure time to the remaining or immigrant subeconomic pest population (Denholm et al., 1983), (4) using selective insecticides that do not exert pressure on other species (both pest and beneficial), and (5) relying on noninsecticidal controls (biological and cultural) that may further reduce the need for pesticide applications. Even when insecticides must be applied, reduced rates may preserve some of the susceptible homozygotes and some beneficial arthropods-which may further reduce the need for subsequent applications (Tabashnik and Croft, 19821. The use of reduced rates, however, may not always provide economic control, and this requires more attentive scouting. Conversely, a tactic for eliminating heterozygotes and resistant homozy- gotes is increased insecticide rates (Taylor and Georghiou, 1979~. Tabashnik and Croft (1982) describe the conditions to determine the choice between the reduced rate (low dose) and increased rate (high dose) approaches. The information required to make an appropriate decision, including genetic data on phenotypic expression in heterozygotes and allele frequency, is generally lacking.
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RESISTANCE IN ARTHROPODS 339 Other chemical approaches may be used to suppress or eliminate resistance alleles from a population. These kill heterozygotes and resistant homozygotes but often require the reintroduction of susceptible individuals, just as the increased dose tactic does. Insecticide mixtures are a common tactic, but to work most effectively the compounds must have different modes of action and metabolism, and the frequencies of resistance alleles to each insecticide must be low. Thus, individuals surviving one insecticide are likely to be killed by the other (Georghiou, 1980b). The common practice with mixtures is to use reduced rates of each insecticide, which sometimes may not be sufficient to delay resistance (Suthert and Comins, 19791. Also, using two insecticides at full rates may be less expensive than using one insecticide at the rate sufficient to kill the heterozygotes. Materials with negative cross-resistance, those that decrease resistance to other chemicals as resistance to them increases, have a potential value in resistance management. Negative cross-resistance has been documented in both Diptera (Ogita, 1961a,b) and Homoptera (Ozaki, 1980~. Although the benefits of negative cross-resistance have not been demonstrated in the field (Sawicki, 1981), they might be most efficient as mixtures. Synergists suppress metabolic resistance mechanisms and, therefore, can prevent or overcome resistance (Ranasinghe and Georghiou, 1979~. (Most resistance management tactics only delay resistance.) Unfortunately, the available synergists have undesirable characteristics, including photoinsta- bility and phytotoxicity. Marketing and registration considerations limit the development of new synergists, and synergists cannot prevent the develop- ment of resistance through alternative means (Oppenoorth, 19764. Where possible, insecticides conferring the lowest level of resistance are preferred, because their use reduces the selective advantages to individuals carrying resistant genotypes (Devonshire and Moores, 19821. Thus, com- pounds causing low levels of resistance delay its development, similar to synergists, because resistant individuals can often be killed with only a slight . . increase in c ose. Treating life stages where genes for metabolic mechanisms of resistance are not expressed (or only poorly expressed) is another direct tactic. For example, Spodoptera littoralis (Boisduval) adults and eggs are more sus- ceptible to organophosphates than larvae, apparently due to higher mi- crosomal cytochrome P4so levels in the larvae (Dittrich et al., 19801. Metabolic forms of resistance can, however, develop in adult arthropods (Plapp, 19761. This tactic would require a major change in the philosophy and mechanics in programs because control is redirected at nondamaging stages. Although an indirect approach, insecticide rotations (alternations) can re- duce resistance allele frequencies, assuming that resistant genotypes have substantially lower fitness than the susceptibles. Therefore, their frequency
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340 TACTICS FOR PREVENTION AND MANAGEMENT declines during generations between applications of the compound (Geor- ghiou, 1980b). Tactical Considerations in insecticide Application Although noninsecticidal controls that indirectly affect resistance devel- opment may become more important in suppressing populations and man- aging resistance, pesticides will continue to be the major control tools in the near future. Pesticide use, however, forces us to choose between mixtures, rotations, and sequences in application (Georghiou, 1980b), and adequate information to confidently choose which tactic to use is lacking. Sequences are normally forced on us by the failure of one compound and the registration of a new compound. Keiding (1977) suggested that insecticides with simple one-factor resis- tance and limited cross-resistance, such as malathion, be used first in a sequence and that compounds with complicated multiple resistance or that act as selectors for resistance to other insecticides, such as dimethoate, be avoided or used last. This information, however, only became available through hindsight (Sawicki, 19751. Whether this information can be auto- matically extrapolated to other systems without recognizing possible meta- bolic differences is questionable. A key assumption about rotations is that resistant genotypes are at a sig- nificant competitive disadvantage in the absence of selection pressure. Al- though resistance usually declines in the absence of a pesticide, the rates of decline may be too slow to be of much practical benefit (Curtis et al., 1978; Georghiou et al., 1983; Roush and Plapp, 1982; Emeka-Ejiofor et al., 19831. Thus, rather than significantly extending the number of times that an insec- ticide can be used, alternation may allow an insecticide to be used only half as often in twice as many seasons. The use of insecticide mixtures is not without problems. Sometimes re- sistance to both compounds used in mixtures has developed rapidly. Some authorities on resistance feel that mixtures should never be used (Keiding, 19771. The potential utility of insecticide mixtures has been investigated experimentally since the early 1950s and has failed in some of these studies (Lagunes, 19801. Other studies have indicated that mixtures are more effec- tive than rotations in preventing resistance development (MacDonald et al., 19831. There are several possible explanations for these inconsistencies. Cross- resistance can occur among some of the pesticides used in the early studies of mixtures. Most field trials were conducted on such a small geographical scale, for example, within an orchard (Asquith, 1964), that resistant indi- viduals in one plot could easily contaminate others. More important, how- ever, most studies were conducted on "closed" laboratory populations, where
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RESISTANCE IN ARTHROPODS 341 there was no immigration of susceptible individuals and where the entire strain was treated in every generation. Various theoretical models (Kable and Jeffery, 1980) indicate that insecticide mixtures can significantly delay resistance development only when a portion of the population of each gen- eration escapes selection. The theoretical models make good sense. If the entire population is treated, only those rare individuals with resistance to both pesticides can survive, and their offspring will be highly resistant. If, however, some susceptible individuals escape treatment, as usually happens, they can greatly dilute the resistance carried by the few individuals that survived the application. More research is needed to define clearly the re- sistance management potential of these pesticide application philosophies. Much of the work necessary for understanding the genetics, biochemistry, physiology, and toxicology of resistance has been conducted on Diptera, primarily the house fly and mosquitoes (Georghiou, 19831. The work has also been valuable in developing a "model" of the general insect system and resistance. It would be dangerous, however, to extrapolate directly to agronomic pests what has been learned on these medically important Dipteral The metabolisms of the house fly and mosquitoes evolved under extremely different selection pressures than those of phytophagous insects (Swain, 1977; Brattsten, 1979a,b) and, therefore, may have different major detoxification pathways. With the relatively recent appreciation of the role different food sources have played in the evolutionary development of metabolic pathways, the necessity for conducting basic resistance research in genetics, biochem- istry, physiology, and toxicology on agronomic pests (e.g., Lepidoptera, Coleoptera, and Acarina) has been advocated (Sawicki, 1981; Metcalf, 19831. CONSTRAINTS ON AUGMENTING TACTICS Implementing the above tactics will be more advantageous if the scientific, economic, and social/political constraints are recognized. The economic and social/political constraints are covered in detail in other papers in this volume (Dover and Croft, Frisbie et al., Miranowski and Carlson). Some trends appear to be eroding the advances made in integrated pest management (IPM), which has serious implications for resistance development. Erosion of Integrated Pest Management In the past, broad-spectrum, long-residual insecticides were applied on a calendar schedule, which continuously exposed both pest and beneficial insect populations. When lead arsenate and DDT were used, calendar spraying was thought to be inexpensive insurance for a quality crop. The first recognized cost added to this practice was the development of resistance and the loss of control within the pest populations. Farmers switched to new insecticides
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342 TACTICS FOR PREVENTION AND MANAGEMENT uncier development and continued on what has been aptly termed the pesticide treadmill (van den Bosch, 1978~. IPM, developed in the mid 1970s, offered the farmer an opportunity to reduce pesticide applications by more critically timing and directing his sprays. The development and evolution of IPM was prompted partly by insecticide resistance. Inasmuch as IPM programs gen- erally reduce pesticide applications, they also minimize resistance selection pressure (Brown, 19811. Although it would be difficult to document, the practice of IPM has surely slowed the development of resistance. Pesticides are a minor portion of total production costs for many high- value crops. In these systems there is always a temptation to use pesticides as cheap insurance, particularly when farmers are in financial difficulty and as memories of past repercussions grow dim. Thus, resistance management gains made in the past may be lost as IPM programs are gradually eroded. For example, recent cotton production practices in the United States (such as early-season insecticide use and area-wide management programs) may be eroding past IPM successes. Certain insecticides, including a pyrethroid, have recently been marketed under "yield enhancement programs"; the prod- uct is guaranteed by the manufacturer to give higher yields when applied to young cotton. Although the mechanism of yield enhancement is unclear, the insecticide seems to affect insects rather than plant physiology. Such mar- keting practices help form convictions among private consultants that eco- nomic thresholds do not work. Also, the risk in this practice is increased selection pressure on cotton pests. An example of an area-wide management program is that of cotton pest management, where insecticides are applied nearly simultaneously across a several square kilometer community when an economic threshold is reached on a central index field that includes less than 0.2 percent of the area (Phillips et al., 19801. How much impact the early season and area-wide insecticide treatment programs will have on cotton pest problems and resistance management is not clear yet. They remind us, however, of the importance of socioeconomic factors on resistance management. Optimum yield for short- and long-term benefits is not always the maximum yield. Resistance Risk Assessment Much scientific understanding has yet to evolve concerning resistance. Until that information and support are available, social or political expediency might force the premature implementation of a program or tactic. An example of this would be to require a resistance risk assessment when registering an insecticide. Currently, appropriate information on resistance development is available only through hindsight. In addition, compounds that have had resistance develop to them tend to maintain some degree of field utility. Although the potential for resistance development should be considered when
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RESISTANCE IN ARTHROPODS 343 choosing an insecticide, it is premature to include risk assessment in the registration process. Detection To select the proper tactic for preventing or managing resistance, we must better understand resistance at the levels of the individual and the population (Sawicki, 19811. Therefore, we must develop methods for detecting resis- tance. Monitoring must be able to detect shifts in susceptibility early in their occurrence within a population. Current monitoring techniques (e.g., topical application, deposit-on-glass, impregnated paper) require large numbers of individuals to detect resistance alleles at low frequencies. This is frequently an impossible task because of sampling constraints, and these methods can become expensive in terms of time and resources. Therefore, techniques to detect rather than document resistance are necessary before we can act, rather than react. Advances have been made in developing bioassays for detecting car- boxylesterase and acetylcholinesterase levels in individual aphids, leaf- hoppers, planthoppers, and mosquitoes (Miyata et al., 1980; Saito and Miyata, 1982; Miyata, 19831. These tests, which are relatively simple and often can be used in the field, provide more effective means for detecting the frequency of a trait within a field population. They also have disad- vantages. A similar test to detect the presence of the most important enzyme system in insecticide detoxification, microsomal oxidases, is cur- rently impossible (L. B. Brattsten, du Font, personal communication, 1984), as are similar tests for the nonmetabolic modes of resistance (e.g., target site insensitivity, penetration, sequestration, excretion). Although the presence of the enzymes can be detected, their levels cannot be de- termined. Further advances in test development are required if we are to begin detecting resistance at low population frequencies, which is required for the proper selection of management tactics. CONCLUSION Our selection of resistance tactics has been dependent on past successes and failures in the field and a great degree of luck. This is unfortunate because ( 1 ) it relies on presupposition rather than scientific fact; (2) the tactic chosen may be inappropriate for the case at hand and may lead to additional com- plications; and (3) tactic selection, implementation, and validation are pri- marily based on reaction rather than calculated action. This realization underscores the critical need for additional basic resistance research in a diverse set of disciplines, including genetics, toxicology, bio- chemistry, and physiology as well as economic entomology. In addition, we
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344 TACTICS FOR PREVENTION AND MANAGEMENT need to validate and further develop for phytophagous insects what we have learned on the house fly and mosquitoes. We need to develop an information matrix on the biology, genetics, and modes and mechanisms of resistance to each insecticide for a broad array of species. This matrix should include species where resistance has not been a problem as well as those where it has been a serious problem. This will be no easy task, and questions of responsibility arise. Who is going to conduct the research? How is it to be funded? Who is going to coordinate it? The action taken on these points by policymakers might ultimately determine the success or futility of pesticide resistance management. ACKNOWLEDGMENT This paper has been approved as No. 5986 by the Director, Mississippi Agricultural and Forestry Experiment Station. REFERENCES Asquith, D. 1964. Resistance to acaricides in the European red mite. J. Econ. Entomol. 57:905- 907. Brattsten, L. B. 1979a. Biochemical defense mechanisms in herbivores against plant allelochemicals. Pp. 199-220 in Herbivores: Their Interaction with Plant Secondary Metabolites, B. A. Rosenthal and D. H. Janzen, eds. New York: Academic Press. Brattsten, L. B. 1979b. Ecological significance of mixed function oxidations. Drug Metab. Rev. 10:35-58. Brown, T. M. 1981. Countermeasures for insecticide resistance. Bull. Entomol. Soc. Am. 27:198- 202. Croft, B. A. 1984. Immigration as an operational factor in resistance management. Paper presented at Pac. Br. Entomol. Soc. Am. Meet., Salt Lake City, Utah, June 19-21, 1984. Curtis, C. F., L. M. Cook, and R. J. Wood. 1978. Selection for and against insecticide resistance and possible methods for inhibiting the evolution of resistance in mosquitoes. Ecol. Entomol. 3:273-287. Denholm, I., A. W. Farnham, K. O'Dell, and R. M. Sawicki. 1983. Factors affecting resistance to insecticides in house flies, Musca domestica L. (Diptera: Muscidae). I. Long-term control with bioresmethrin of flies with pyrethroid-resistance potential. Bull. Entomol. Res. 73:481-489. Devonshire, A. L., and G. D. Moores. 1982. A carboxylesterase with broad substrate specificity causes organophosphorus, carbamate and pyrethroid resistance in peach-potato aphids (Myzus persicae). Pestic. Biochem. Physiol. 18:235-246. Dittrich, V., N. Luetkemeier, and G. Voss. 1980. OP-resistance in Spodoptera littoralis: Inheritance, larval and imaginal expression, and consequences for control. J. Econ. Entomol. 73:356-362. Emeka-Ejiofor, S. A. I., C. F. Curtis, and G. Davidson. 1983. Tests for effects of insecticide resistance genes in Anopheles gambiae on fitness in the absence of insecticides. Entomol. Exp. Appl. 34: 163- 168. Futuyma, D. J. 1979. Evolutionary Biology. Sunderland, England: Sinauer Associates. Georghiou, G. P. 1980a. Insecticide resistance and prospects for its management. Residue Rev. 76:131-145. Georghiou, G. P. 1980b. Implications of the development of resistance to pesticides: Basic principles
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RESISTANCE IN ARTHROPODS 345 and consideration of countermeasures. Pp. 116-129 in Pest and Pesticide Management in the Caribbean. Proc. Seminar and Workshop, E. G. B. Gooding, ed. Berkeley, Calif.: Consort. Int. Crop Prot. Georghiou, G. P. 1983. Management of resistance in arthropods. Pp. 769-792 in Pest Resistance to Pesticides, G. P. Georghiou and T. Saito, eds. New York: Plenum. Georghiou, G. P., and C. E. Taylor. 1977a. Genetic and biological influences in the evolution of insecticide resistance. J. Econ. Entomol. 70:319-323. Georghiou, G. P., and C. E. Taylor. 1977b. Operational influences in the evolution of insecticide resistance. J. Econ. Entomol. 70:653-658. Georghiou, G. P., A. Lagunes, and J. D. Baker. 1983. Effect of insecticide rotations on evolution of resistance. Pp. 183-189 in IUPAC Pesticide Chemistry, Human Welfare and the Environment, J. Miyamoto, ed. New York: Pergamon. Kable, P. F., and H. Jeffery. 1980. Selection for tolerance in organisms exposed to sprays of biocide mixtures: A theoretical model. Phytopathology 70:8-12. Karban, R., and J. R. Carey. 1984. Induced resistance of cotton seedlings to mites. Science 225:53- 54. Keiding, J. 1977. Resistance in the housefly in Denmark and elsewhere. Pp. 261-302 in Pesticide Management and Insecticide Resistance, D. L. Watson and A. W. A. Brown, eds. New York: Academic Press. Lagunes, A. 1980. Impact of the use of mixtures and sequences of insecticides in the evolution of resistance in Culex quinquefasciatus Say. (Diptera: Culicidae). Ph.D. disseration. University of California, Riverside. Laster, M. L. 1972. Interspecific hybridization of Heliothis virescens and H. subflexa. Environ. Entomol. 1 :682-687. MacDonald, R. S., G. A. Surgeoner, K. R. Solomon, and C. R. Harris. 1983.\Laboratory studies on the effect of four spray regimes on the development of resistance to permethrin and dichlorvos in the house fly. J. Econ. Entomol. 76:417-422. Martinez-Carrillo, J. L., and H. T. Reynolds. 1983. Dosage-mortality studies with pyrethroids and other insecticides on the tobacco budworm (Lepidoptera: Noctuidae) from the Imperial Valley, California. J. Econ. Entomol. 76:983-986. Metcalf, R. L. 1983. Implications and prognosis of resistance to insecticides. Pp. 703-733 in Pest Resistance to Pesticides, G. P. Georghiou and T. Saito, eds. New York: Plenum. Miyata, T. 1983. Detection and monitoring for resistance in arthropods based on biochemical characteristics. Pp. 99-116 in Pest Resistance to Pesticides, G. P. Georghiou and T. Saito, eds. New York: Plenum. Miyata, T., T. Saito, H. Hama, T. Iwata, and K. Ozaki. 1980. A new and simple detection method for carbamate resistance in the green rice leafhopper, Nephotettix cincticeps Uhler (Hemiptera: Deltocephalidae). Appl. Entomol. Zool. 15:351-352. Ogita, Z. 1961a. An attempt to reduce and increase insecticide-resistance in D. melanogaster by selection pressure. Genetical and biochemical studies on negatively correlated cross-resistance in Drosophila melanogaster. I. Botyu-Kagaku 26:7-18. Ogita, Z. 1961b. Genetic studies on actions of mixed insecticides with negatively correlated sub- stances. Genetical and biochemical studies on negatively correlated cross-resistance in Drosophila melanogaster. III. Botyu-Kagaku 26:88-93. \ Oppenoorth, F. J. 1976. Development of resistance to insecticides. Pp. 41-59 in The Future for Insecticides, R. L. Metcalf and J. J. McKelvey, Jr., eds. New York: John Wiley and Sons. Ozaki, K. 1980. Resistance of rice insect pests to insecticides in Japan. Presented at the 16th Int. Congr. Entomol. Kyoto, Japan, August 3-9, 1980. Phillips, J. R., A. P. Gutierrez, and P. L. Adkisson. 1980. General accomplishments toward better insect control in cotton. Pp. 123-153 in New Technology of Pest Control, L. B. Huffaker, ed. New York: John Wiley and Sons.
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346 TACTICS FOR PREVENTION AND MANAGEMENT Plapp, F. W., Jr. 1976. Biochemical genetics of insecticide resistance. Annul Rev. Entomol. 21: 179- 197. Proshold, F. I., D. F. Martin, M.L. Laster, J. R. Raulston, and A. N. Sparks. 1983. Release of backcross insects on St. Croix to suppress the tobacco budworm (Lepidoptera: Noctuidae): Meth- odology and dispersal of backcross insects. J. Econ. Entomol. 76:885-891. Ranasinghe, L. E., and G. P. Georghiou. 1979. Comparative modification of insecticide-resistant spectrum of Culex pipiens fatigans Wied. by selection with temephos and temephos/synergist combinations. Pestic. Sci. 10:502-508. Roush, R. T., and F. W. Plapp, Jr. 1982. Effects of insecticide resistance on biotic potential of the house fly (Diptera: Muscidae). J. Econ. Entomol. 75:708-713. Saito, T., and T. Miyata. 1982. Studies on insecticide resistance in Nephotettix cincticeps. Pp. 377- 382 in Proc. Int. Conf. Plant Prot. in Tropics, K. L. Heong, B. S. Lee, T. M. Lim, C. H. Tech, and Yusof Ibrahim, eds. Kuala Lumpur: Malaysian Plant Protection Society. Sawicki, R. M. 1975. Effects of sequential resistance on pesticide management. Pp. 799-811 in Proc. 8th Br. Insectic. Fungic. Conf. Suffolk: Lavenham. Sawicki, R. M. 1981. Problems in countering resistance. Philos. Trans. R. Soc. London, Ser. B 295:143-151. Sparks, T. C. 1981. Development of insecticide resistance in Heliothis zea and Heliothis virescens in North America. Bull. Entomol. Soc. Am. 27:186-192. Sutherst, R. W., and H. N. Comins. 1979. The management of acaricide resistance in the cattle tick, Boophilis microplus (Canestrini) (Acari: Ixodidae), in Australia. Bull. Entomol. Res. 69:519- 537. Swain, T. 1977. The effects of plant secondary products on insect plant co-evolution. Pp. 249-256 in Proc. 15th Int. Congr. of Entomol., Washington, D.C. College Park, Md.: Entomological Society of America. Tabashnik, B. E., and B. A. Croft. 1982. Managing pesticide resistance in crop-arthropod complexes: Interactions between biological and operational factors. Environ. Entomol. 11:1137-1144. Taylor, C. E., and G. P. Georghiou. 1979. Suppression of insecticide resistance by alteration of gene dominance and migration. J. Econ. Entomol. 72:105-109. van den Bosch, R. 1978. The Pesticide Conspiracy. New York: Doubleday. Wood, R. J., and J. A. Bishop. 1981. Insecticide resistance: Populations and evolution. Pp. 97- 127 in Genetic Consequences of Man Made Change, J. A. Bishop and L. M. Cook, eds. New York: Academic Press.
Representative terms from entire chapter: