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Pesticide Resistance: Strategies and Tactics for Management. 1986. National Academy Press, Washington, D.C. The Magnitude of the Resistance Problem GEORGE P. GEORGHIOU The phenomenon of pest resistance to pesticides has expanded and intensified considerably in recent years. Resistance is most acute in insects and mites, among which at least 447 species- including most major pests have been reported to be resistant to one or more classes of chemicals. At least 23 species are known to have developed resistance to pyrethroids, the most recently introduced class of in- secticides. Whereas the presence of resistance was a rare phenom- enon during the early l950s, it is the fully susceptible population that is rare in the 1980s. Serious cases of resistance are also found in plant pathogens towardfungicides and bactericides and are being reported with increasing frequency in weeds toward herbicides and in rats toward rodenticides. Unquestionably the phenomenon of re- sistance has come to pose a serious obstacle to the efforts of many countries to increase agricultural production and to reduce the threat of vector-borne diseases. What is urgently needed is interdisciplinary research to increase our understanding of resistance and develop practical measures for its management. INTRODUCTION A great variety of arthropods, pathogens, and weeds compete with us for the crops that we grow for our sustenance. In turn, we attempt to control the depredation of these pests by suppressing their densities, often by the use of chemical toxicants. The use of toxicants is not a human innovation. Natural chemical defense mechanisms are present within most of our crop plants, serving to repel or kill many of the organisms that attack them. 14
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MAGNITUDE OF THE RESISTANCE PROBLEM 15 Through the millions of years of life on earth, a continuous process of mutual evolution has taken place between plant and animal species and the various organisms that feed on them. The host plants or animals have evolved defensive mechanisms, including chemical repellents and toxins, exploiting weaknesses in the attacking organisms. In turn the attacking organisms have evolved mechanisms that enable them to detoxify or otherwise resist the defensive chemicals of their hosts. Thus, it appears that the gene pool of most of our pest species already contains genes that enable the pests to degrade enzymatically or otherwise circumvent the toxic effect of many types of chemicals that we have developed as modern pesticides. These genes may have been retained at various frequencies as part of the genetic memory of the species. Resistance of insects to insecticides has a history of nearly 76 years, but its greatest increase and strongest impact have occurred during the last 40 years, following the discovery and extensive use of synthetic organic insec- ticides and acaricides. Resistance in plant pathogens is of more recent origin, the first case having been detected 44 years ago (Farkas and Aman, 1940~. Numerous cases of resistance in these organisms have been reported during the last 15 years, however, coincident with the introduction of systemic fungicides (Georgopoulos and Zaracovitis, 1967; Dekker, 1972; Ogawa et al., 19831. Resistance in noxious weeds is more recent (Ryan, 1970; Ra- dosevich, 1983), but it is now being detected with increasing frequency in species that have been intensively treated with herbicides (LeBaron and Gressel, 1982~. Pesticide resistance is also manifested worldwide in rats species that during history have come to be associated with empty granaries and the bubonic plague. The problem of resistance to pesticides has been the subject of several recent reviews (Dekker and Georgopoulos, 1982; LeBaron and Gressel, 19821. The Board on Agriculture's symposium on "Pesticide Resistance Manage- ment" came almost exactly 33 years after a similar symposium on "Insec- ticide Resistance and Insect Physiology" was convened by the National Academy of Sciences on December 8-9, 1951 (NAS, 1951~. That pioneering symposium, which took place only four years after the first published report of resistance to DDT (Weismann, 1947), was evidence of considerable fore- sight and has paid dividends during the years that followed. Attention, how- ever, was soon directed toward more exciting goals: walking on the moon and probing the planets and beyond. Meanwhile, pests at home and in the fields have continued to evolve biologically toward greater fitness in their chemically altered environments. Whereas the presence of resistance was a rare phenomenon during the early 1950s, it is the fully susceptible population that is rare in the 1980s. Unquestionably the phenomenon of resistance poses a serious obstacle to efforts to increase agricultural production and to reduce or eliminate the threat of vector-borne diseases.
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16 INTRODUCTION I shall attempt to discuss briefly the magnitude of the problem as it exists today, and I hope to convey the urgent need for interdisciplinary effort in the search for greater understanding of resistance to pesticides and practical measures for its management. STATUS OF RESISTANCE The interdisciplinary nature of the problem is evident in the variety of living organisms that have developed resistance and the many types of chem- icals that are involved (Figure 11. It is also apparent that insecticides, being broad-spectrum biocides, have exceeded their intended targets and have se- lected for resistance not only in insects and mites but in practically every other type of organism, from bacteria to mammals. Since genetic resistance cannot be induced by any means other than lethal action, the environmental impact of such unintentional selection may be profound. The chronological documentation of resistance that we have been main- taining at the University of California, Riverside (Figure 2), now indicates that resistance to one or more insecticides has been reported in at least 447 species of insects and mites. In addition at least 100 species of plant pathogens (J. M. Ogawa, University of California, Davis, personal communication, 1984), 48 species of weeds (LeBaron, 1984; H. M. LeBaron, Ciba-Geigy BACTERIA - ORGAN ISM C/ ~'~ ~ SPOROZOA F UNGI NEMATODES . ACARI NA INSECTA CRUSTACE A FISH 1 1 FROGS 1 I RODENTS I WEEDS 1 FIGURE 1 The relative frequency of resistance to xenobiotics.
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MAGNITUDE OF THE RESISTANCE PROBLEM 450 400 350 300 in LU 200 By cr) 1 00 50 · ARTHROPODS o PL ANT PATHOGENS WEEDS NEMATODES _ ~ i 1 1 , 1 to ye O ·~ 1908 1940 50 60 70 80 84 YEARS FIGURE 2 Chronological increase in number of cases of resistant species. 17 Corporation, personal communication, 1984), and 2 species of nematodes (Georghiou and Saito, 1983) have evolved resistance to pesticides (Figure 21. Not shown in Figure 2 are the cases of resistance in rodents, which, according to W. B. Jackson (Bowling Green State University, personal com- munication, 1984), now involve five species. Resistance to the anticoagulant rodenticide warfarin was first reported in 1958 in the Norway rat (Rattus norvegicus) in Scotland (World Health Or- ganization, 19761. In the United States, warfarin resistance in this species was found in North Carolina in 1970 (Jackson et al., 19711. By the mid- 1970s it was detected in at least 25 percent of the sites sampled in the United States (Jackson and Ashton, 19804; at the original site in North Carolina, it occurred in essentially 100 percent of Norway rats, a truly remarkable rate of chemical selection involving a mammal. These data concern cases of resistance that have arisen as a result of the field application of pesticides; they do not include resistance developed in laboratories through simulated selection pressure. The actual incidence of resistance must be higher than is revealed by these records, since resistance is monitored in only a few laboratories and many cases undoubtedly are not reported. Although the rate of increase in resistant species of weeds has accelerated
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18 INTRODUCTION TABLE 1 Increase in Cases of Resistance to Insecticides, 1980-1984a Percent 19801984 Increase . . . Resistant species 428 447 4.4 Species x insecticide classes affectedb 829 866 4.1 Species x insecticides 1,640 1,797 9.4 Species x insecticides x countries of occurrence 3,675 3,894 5.9 aOctober 1984. Data for 1980 from Georghiou, 1981. bClasses: DDT, dieldr~n, organophosphate, carbamate, pyrethroid, fumigant, miscellaneous. SOURCE: Georghiou, 1981; Georghiou, unpublished. since 1980, the rate of increase in resistant species of arthropods has declined. The reason for this decline is that an increasingly large proportion of new cases of resistance to insecticides now involves species that were recorded previously as resistant to earlier pesticides. A more realistic impression of the trend in insecticide resistance can be obtained when the increase since 1980 is viewed as the number of different insecticides to which each species is reported to be resistant. This analysis shows an increase of 9.4 percent versus a 4.4 percent rise in the number of new resistant species (Table 11. The distribution of known cases of resistance among different orders of arthropods and the classes of chemical groups involved is indicated in Table 2. Of the 447 species concerned, 59 percent are of agricultural importance, 38 percent are of medical or veterinary importance, and 3 percent are ben- eficial parasites or predators. Resistance is most frequently seen in the Diptera (156 species, or 35 percent of the total), reflecting the strong chemical selection pressure that has been applied against mosquitoes throughout the world. Substantial numbers of resistant species are also evident in such agriculturally important orders as the Lepidoptera (67 species, 15 percent), Coleoptera (66 species, 15 percent), Acarina (58 species, 13 percent), Homoptera (46 species, 10 percent), and Heteroptera (20 species, 4 percent). The resistant species include many of the major pests, since it is against these that chemical control is mainly directed. With regard to chemical groups, cyclodiene insecticide resistance is found in 62 percent of the reported species and DDT resistance in 52 percent, followed closely by organophosphate resistance in 47 percent. Lower per- centages are reported for the more recently introduced carbamate and pyr- ethroid insecticides. The high frequency of organophosphate resistance is undoubtedly due to the widespread use of these insecticides. It is perhaps ironic that one of the reasons organophosphates were considered more de- sirable than organochlorines was the prospect that these compounds, having relatively shorter persistence, would be less efficient selectors for resistance.
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20 INTRODUCTION TABLE 3 Number of Species of Insects and Mites at Various Stages of Multiple Resistance Year Number of Classes of Insecticidesa Resistant that Can Be Resisted Species 1 2 3 4 5 1938b 77 0 0 0 0 1948b 1413 1 0 0 0 1955C 254 18 3 0 0 1969b 224155 42 23 4 0 1976d 364221 70 44 22 7 1980e 428245 95 53 25 10 1984f 447234 ~ 19 54 23 17 aDDT, cyclodienes, organophosphates, carbamates, pyrethroids. bBrown (1971). CMetcalf (1983). Georghiou and Taylor (1976). eGeorghiou (1981). fRecords through October 1984. SOURCE: See notes above; 1984 material new to this document. For plant pathogens, the compilation of Ogawa et al. (1983) indicated that of the 70 species of fungi reported as resistant by 1979, 59 species (84 percent) were resistant to the systemic fungicide benomyl. Other, smaller categories involved thiophanate resistance (in 13 species of fungi) and strep- tomycin resistance (in 8 species of bacteria). Among weeds most instances of resistance (41 species 28 dicots and 13 monocots) involve resistance to the triazine herbicides. In addition at least seven weed species are resistant to other herbicides, including phenoxys (e.g., 2,4-D), trifluralin, paraquat, and ureas. Of considerable importance in exacerbating the magnitude of the resistance problem is the ability of a given population to accumulate several mechanisms of resistance. None of the present mechanisms known in field populations excludes any other mechanism from evolving. Despite the search for pairs of compounds with negatively correlated resistance, none has been discovered that would have the potential for field application. The coexistence of several resistance mechanisms (each affecting different groups of chemicals), re- ferred to as multiresistance, has become an increasingly common phenom- enon. Now almost half of the reported arthropod species can resist compounds in two, three, four, or five classes of chemicals (Table 31. Seventeen insect species can resist all five classes, including the relatively new class of py- rethroid insecticides. The species that have developed strains resistant to pyrethroids (Table 4) include some of our most important pests, such as the Colorado potato beetle (Leptinotarsa decemlineata) in Long Island, New
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MAGNITUDE OF THE RESISTANCE PROBLEM 21 York, New Jersey, Pennsylvania, and Rhode Island; the malaria vectors Anopheles albimanus in Central America and An. sacharovi in Turkey; the house fly (Musca domestica) in several countries; white flies (Bemisia tabaci) on cotton in California; the virus vector aphid Myzus persicae in a number of countries; several lepidopterous pests of cotton and other crops (Heliothis, Spodoptera); and Plutelia xylostella, a diamondback moth that is a major pest of cole crops in southeast Asia and elsewhere. Resistance to pyrethroids has often evolved rapidly on the foundation of DDT resistance. It has been clearly demonstrated toxicologically, genetically (Omer et al., 1980; Priester and Georghiou, 1980; Malcolm, 1983), and electrophysiologically (Miller et al., 1983) that a semirecessive gene, kdr, often- detected as one of the components of DDT resistance, is also selected by and provides protection against pyrethroid insecticides. Pyrethroid resis- tance that includes this gene is characteristically high, often exceeding 1,000- fold in kdr homozygotes, thus effectively precluding further use of pyreth- roids against these resistant populations. There is valid concern that the effective life span of pyrethroids may be shorter in many developing coun- tries, where their use directly succeeded that of DDT, than it will be in many developed countries, where the sequence after DDT has involved several years of organophosphate and carbamate use. As in arthropods the range of compounds to which plant pathogenic fungi are resistant has expanded to include representatives of the more recently developed fungicides. Figure 3 indicates the progressive growth of fungicide resistance since 1960, with the inclusion during the last four years of cases of resistance to the dicarboximides, dichloroanilines, acylalanines, and er- gosterol biosynthesis inhibitors. FREQUENCY AND EXTENT OF RESISTANCE When considering the magnitude of the problem, it is necessary to draw attention to the many cases of widely distributed resistance and to the high frequency of resistance genes in populations. The most frequently observed pattern of the spread of resistance is one in which isolated cases appear, initially creating a mosaic pattern that reflects the distribution and degree of selection pressure. As resistance "ages," that pattern is gradually obscured by insect dispersal and by the more widespread application of selection pressure. In the Imperial Valley of California the pattern of resistance of the white fly Bemisia tabaci toward the new pyrethroid insecticides is still distinct, reflecting the number of pyrethroid treatments applied to cotton during 1984 (Figure 4~. In coastal southern France the high frequency of organophosphate resistance found in Culex pipiens reflects the very intense chemical control
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24 198 1-84 35t 30 Ad LLI 2 5 En En I1J ~ 15 F 20 10 _ ~ '2-''T'::' He 5 -Am_ //////////// A:::: .:::::-:-:::-,:-:: .:-::::: r I 1960 INTRODUCTION DICARBOXYMIDES DICHLOROANILINES ACYLALANINES ERGOSTEROL BIOSYNTHESIS INHIBITORS ORGANICPHOSPHATES ORGANIC TIN CARBOXAM I DES ANTIBIOTICS BENZ IMIDAZOL ES PYRIMIDINES DODINE AROMATIC HYDROCARBONS MERCURIALS 1970 1980PHT~ALlM:DEs COPPE R SUL FUR FIGURE 3 History of resistance to chemicals in plant pathogens. Source: Delp (1979), adapted from Dekker (1972), Georgopoulos (1976), and Ogawa et al. (1977); additional data from Dekker and Georgopoulos (1982) and J. M. Ogawa, University of California, Davis, personal communication, 1984. that is being applied to protect this urbanized area. The frequency of resistance declines in the interior. Under prolonged and intensive selection the frequency of resistance sta- bilizes and may show a surprising uniformity. In Great Britain, high resistance to demeton S-methyl was found uniformly in yearly samples of the hops aphid Phorodon humuli obtained from Kent during 1966-1976, compared with a susceptible population from north England during 1969-1976 (Figure 51. In another survey, involving 258 collections of the green peach aphid, only 3 collections did not contain dimethoate-resistant individuals; in 197 of the collections, more than 76 percent of the aphids were resistant (Sawicki et al., 19781. A generally uniform pattern is evident in the distribution of resistance of
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34 INTRODUCTION 250 LL ~ 200 ~L I LLJ I 50 cn y I 100 I1J C) 50 5.8 x ~ SUMMER OIL OMETHOATE Dl N OCAP OME T HOATE 5.1 x 3.9 x 2.4 x Ix PARATHION _ DE ME TON - S-METH YL CHLORPHENAMI DINE + FORMETANATE DIAZINON + PHENKAPTON RESISTANCE IN EUROPEAN RED MITE FIGURE 1 1 Increasing control effort and costs as pesticide resistance increases in the European red mite. Source: Steiner (1973~. TABLE 7 Development of Resistance to Aldicarb, Fenvalerate, and Synergized Fenvalerate in a Long Island Population of Colorado Potato Beetle Resistance Factor at LDso Fenvalerate Piperonyl Year Generation Aldicarb Fenvalerate butoxide 1980 Overwintering - 20 x First 13x 30x Second 22 x 100 x 1981 Overwintering 9 x 30 x 1.3 x First 33 x Second 33 x 130x 4x 1982 First 130x 4x Second 60 x >600 x 1983 Overwintering >600 x 200 x First >600x 200x SOURCE: Forgash, 1984b.
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MAGNITUDE OF THE RESISTANCE PROBLEM TABLE 8 Relative Costs of Insecticides for Residual House Spraying 35 Approximate Dosage residual effect glm2 (tech.) months Cost per kga $0.33 Cost per b $0.34 l.oa Relative cost per 6 months DDT 2.0 75% wp Dieldrin 50% wp Lindane 50% wp Malathion 50% wp Propoxur 50% wp Fenitrothion 40% wp Deltamethrin 5% wp 0.5 0.5 2.0 2.0 2.0 3 2.63 0.1 2.34 1.7 3.45 5.1 0.89 1.02 5.3a 3.40 20.4a 1S.ga ~$so.oo l4.6b NOTE: wp = wettable powder. aWorld Health Organization data; Wright et al. (1972); Fontaine et al. (1978). bEstimated from relative wholesale price of technical compound, Metcalf (1983). SOURCE: Metcalf (1983). Therefore, it is not surprising that the rate of introduction of new pes- ticides declined precipitously between 1970 and 1980 (Figure 13J. Al- though several factors may have been responsible for this decline, it is strongly suspected that industry frustration with resistance has played an important role. The question may be posed, therefore, whether we have already selected TABLE 9 Estimated Environmental Costs Due to Loss of Natural Enemies and Insecticide Resistance in Pest Insect and Mite Populations Total Added Insecticide Costs ($) Due to Loss of Natural Enemies Increased Resistance Field crops133,007,000101,810,000 Vegetable crops6,235,0007,958,000 Fruits and nuts14,242,0008,312,000 Livestock and public health>015,000,000 Total153,484,000133,080,000 SOURCE: Pimentel et al. (1979).
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36 1 8 16 _ la _ INTRODUCTION 20 a CHANCES FOR SUCCESS /0 E 12 - 10 8 o 6 4 _ 2 _~ O 1,,,,,,, 1,,,, 1, 1,,, 1,,,,,,,, 1, 1956 1964 1969 1971 1975 1984 O~ C C COST (8 milt) ! /1 000 1/5000 En 10,000 It) Cal 5,000 ~ 20000 try ' cr 1 /251OOO LL 1/30,000 ct. 1 / 35,000 <' 1 /40,000 (A 1 /4s,000 50,000 FIGURE 12 Estimated cost of developing an agricultural chemical and chance for a new chemical to become a product. Source: Mullison (1976) and others. in pests all the various oxidases, esterases, glutathione transferases, dehy- drochlorinases, and other enzyme systems that may enable them to quickly evolve resistance to practically any toxicant that may be used against them. The answer will be provided in time by the pests themselves. This concern has not deterred the search for new chemical weapons, however (Magee et al., 19841. The new emphasis is characterized by a more rational approach. for 91 8 7 6 5 4 3 2 HERBICIDES F UNG IC IDES · - - INSECTICIDES ~ 1.-'\\ 1940 1950 FIGURE 13 Annual introduction of new pesticides during the period 1940-1980. Source: Martin and Worthing (1977), Worthing (1979), Patton et al. (1982). it,, ~ .l .. ; a, ~1 lo- .1 I 960 1 970 1980
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MAGNITUDE OF THE RESISTANCE PROBLEM TABLE 10 Chronology of Insecticide Discoveries 37 Decade Discovery 1940s l950s 960s 970s 980s Chlorinated hydrocarbons: DDT, BHC, apron, chlordane, toxaphene OPS: parathion, methyl parathion Carbamates: isolan, dimetilan OPS: malathion, azinphosmethyl, phorate, vinyl phosphates Carbamates: carbaryl OPS: fonofos, tr~chloronate Carbamates: carbofuran, aldicarb, methomyl Pyrethroids: resmethrin Formamidines: chlordimeform Pyrethroids: permethrin, cypermethrin, deltamethrin, fenvalerate New OPs: terbufos, methamidophos, acephate New Carbamates: bendiocarb, thiofanox IGRs: methoprene, diflubenzuron AChE receptor blockers: cartap New Pyrethroids: flucythrinate Procarbamates: carbosulfan, thiodicarb New IGRs: phenoxycarb Microbials: BT, BTI, Bacillus sphaericus AChE receptor blockers: bensultap GABA agonists: milbemycin, avermectin Miscellaneous: AMDRO, cyromazine SOURCE: Adapted in part from Menn (1980). Some of these chemicals are the result of optimization of structures within the existing classes of insecticides, such as new pyrethroids, procarbamates, and insect growth regulators. Others are totally novel, having had the* genesis in the progress that is being made in our understanding of basic biology, biochemistry, and physiology, at both the organismal and molecular levels. Representatives of this effort are the acetylcholinesterase receptor blockers, the GABA agonists, and a number of other compounds such as AMDRO and cyromazine (Table 101. Evidence of rekindled interest is seen in the small but perceptible increase in the number of new insecticides submitted to the World Health Organization for testing against mosquito and other vector species, after a strong decline in such submissions during the 1970s (Figure 141. Likewise, we now see an increased interest in research on insecticide resistance, as evidenced by the percentage of resistance papers published in the Journal of Economic En- tomology (Figure 151.
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38 INTRODUCTION 100 90 _ En LLI O 80 C, o 70 _ o 60 En: LLI Lo a) 40 ~0 ~ 30 En LLI 1 RESISTANT / MOSQUITO / SPECIES -A/ 20 10 _ to ~ NEW / ' , INSECTICIDES _ Jo. 1940 '50 '60 '70 '80 W _ t _ .. YEARS 60 C) 50 in 40 30 Id In Z FIGURE 14 Numbers of new insecticides submitted for testing to the World Health Organization, 1960-1984, compared with the appearance of resistance in mosquito spe- cies. Source: Georghiou, unpublished. The problem is evident, the need for action is compelling, and the op- portunities for breakthroughs are substantial. It has always been axiomatic that one must intimately know one's enemy to be able to defeat him. I hope that this conference, through its exploration of the nature of pesticide resis- tance from all known perspectives, will enable us to develop the means and strategies for countering the adverse impact of this phenomenon on our well- being.
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MAGNITUDE OF THE RESISTANCE PROBLEM 450 400 350 En LL] ~ 250 11 o 300 200 m 150 As 100 50 _ RESISTANT SPECIES f OF ARTHROPODA ~ t O _ ~ i, ~ ~I I I r 10 - PAPERS ON RESISTANCE 8 - IN J.E.E. (%) FEZ , ~ . ~ 1908 1940 50 60 70 80 84 39 FIGURE 15 Percentage of papers concerned with insecticide resistance published in the Journal of Economic Entomology, 1945-1983, compared with the evolution of resistance in species of Arthropoda. Source: Georghiou, unpublished. REFERENCES Attia, F. I., and J. T. Hamilton. 1978. Insecticide resistance in Myzus persicae in Australia. J. Econ. Entomol. 71:851-8S3. Braunholtz, J. T. 1981. Crop protection: The role of the chemical industry in an uncertain future. Philos. Trans. R. Soc. London, Ser. B 295:19-34. Brown, A. W. A. 1971. Pest resistance to pesticides. Pp. 457-552 in Pesticides in the Environment, Vol. 1, Part II, R. White-Stevens, ed. New York: Marcel Dekker.
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40 INTRODUCTION Campbell, C. J., and D. G. Finlayson. 1976. Comparative efficacy of insecticides against tuber flea beetle and aphids in potatoes in British Columbia. Can. J. Plant Sci. 56:869-875. Champ, B. R., and M. J. Campbell-Brown. 1970. Insecticide resistance in Australian Tribolium castaneum (Herbs") (Coleoptera: Tenebrionidae). II. Malathion resistance in eastern Australia. J. Stored Prod. Res. 6:111- 131. Craig, I. A., G. P. Conway, and G. A. Norton. 1982. The consequences of resistance. Pp. 43-60 in Pesticide Resistance and World Food Production, G. Conway, ed. London: Imperial College, Mineral Resources Engineering Department. Davidson, G. 1980. Insecticide resistance in Old World anopheline mosquitoes. World Health Organization Unpubl. Doc. VBC/EC/80.4. Dekker, J. 1972. Resistance. Pp. 156-174 in Systemic Fungicides, E. Marsh, ed. New York: John Wiley and Sons. Dekker, J., and S. G. Georgopoulos, eds. 1982. Fungicide Resistance in Crop Protection. Wag- eningen, Netherlands: Centre for Agricultural Publishing and Documentation. Delp, C. J. 1979. Resistance to plant disease control agents: How to cope with it. Pp. 253-261 in Proc. 9th Int. Congr. Plant Prot., Vol. 1, T. Kommedahl, ed. Minneapolis, Minn.: Burgess. El-Guindy, M. A., S. M. Madi, M. E. Keddis, Y. H. Issan, and M. M. Abdel-Satto. 1982. Development of resistance to pyrethroids in field populations of the Egyptian cotton leafworm, Spodoptera littoralis Boisd. Int. Pest Control 24(1):6,8,10-11,16-17. Farkas, A., and J. Aman. 1940. The action of diphenyl on Penicillium and Diplodia moulds. Palest. J. Bot. Jerusalem Ser. 2:38-45. Fontaine, R. E., J. H. Pull, D. Payne, G. D. Pradhan, G. P. Joshi, J. A. Pearson, M. K. Thymakis, and M. E. Ramos Camacho. 1978. Evaluation of fenitrothion for the control of malaria. Bull. W.H.O. 56:445-452. Forgash, A. J. 1981. Insecticide resistance of the Colorado potato beetle, Leptinotarsa decemlineata (Say). Pp. 34-46 in Advances in Potato Pest Management, J. W. Lashomb and R. Casagrande, eds. Stroudsburg, Pa.: Hutchinson Ross. Forgash, A. J. 1984a. History, evolution, and consequences of insecticide resistance. Pestic. Biochem. Physiol. 22:178-186. Forgash, A. J. 1984b. Insecticide resistance of the Colorado potato beetle, Leptinotarsa decemlineata (Say). Paper presented at 17th Int. Congr. Entomol., Hamburg, Federal Republic of Germany, August 1984. Gauthier, N. L., R. N. Hofmaster, and M. Semel. 1981. History of Colorado potato beetle control. Pp. 13-33 in Advances in Potato Pest Management, J. H. Lashomb and R. Casagrande, eds. Stroudsburg, Pa.: Hutchinson Ross. Georghiou, G. P. 1980. Insecticide resistance and prospects for its management. Residue Rev. 76:131-145. Georghiou, G. P. 1981. The occurrence of resistance to pesticides in arthropods: An index of cases reported through 1980. Rome: Food and Agriculture Organization of the United Nations. Georghiou, G. P. 1982. The implication of agricultural insecticides in the development of resistance by mosquitoes with emphasis on Central America. Pp. 95-121 in Resistance to Insecticides Used in Public Health and Agriculture. Proc. Int. Workshop, 22-28 February, 1982. Colombo, Sri Lanka: Nat. Sci. Council Sri Lanka. Georghiou, G. P., and R. Mellon. 1983. Pesticide resistance in time and space. Pp. 1-46 in Pest Resistance to Pesticides, G. P. Georghiou and T. Saito, eds. New York: Plenum. Georghiou, G. P., and T. Saito, eds. 1983. Pest Resistance to Pesticides. New York: Plenum. Georghiou, G. P., and C. E. Taylor. 1976. Pesticide resistance as an evolutionary phenomenon. Pp. 759-785 in Proc. 15th Int. Cong. Entomol., Washington, D.C. College Park, Md.: Ento- mological Society of America. Georghiou, G. P., S. G. Breeland, and V. Ariaratnam. 1973. Seasonal escalation of organophos- phorus and carbamate resistance in Anopheles albimanus by agricultural sprays. Environ. Entomol. 2:369-374.
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MAGNITUDE OF THE RESISTANCE PROBLEM 41 Georgopoulos, S. G. 1976. Mutational resistance to site-specific fungicides. Pp. 1057-1061 in Proc. 3rd Int. Biodegrad. Symp., J. M. Sharpley and A. M. Kaplan, eds. London: Applied Science Publishers, Ltd. Georgopoulos, S. G., and C. Zaracovitis. 1967. Tolerance of fungi to organic fungicides. Annul Rev. Phytopathol. 5: 109-130. Gunning, R. V., C. S. Easton, L. R. Greenup, and V. E. Edge. 1984. Pyrethroid resistance in Heliothis armiger (Hubner) (Lepidoptera: Noctuidae) in Australia. J. Econ. Entomol. 77:1283-1287. Ho, S. H., B. H. Lee, and D. Lee. 1983. Toxicity of deltamethrin and cypermethrin to the larvae of the diamondback moth, Plutella xylostella. Toxicol. Lett. 19:127-131. Hobbs, J. H. 1973. Effect of agricultural spraying on Anopheles albimanus densities in a coastal area of El Salvador. Mosq. News 33:420-423. Jackson, W. B., and A. D. Ashton. 1980. Vitamin K-metabolism and vitamin K-dependent proteins. 8th Steenbock Symp., J. W. Suttie, ed. Baltimore, Md.: University Park Press. Jackson, W. B., P. J. Spear, and C. G. Wright. 1971. Resistance of Norway rats to anticoagulant rodenticides confirmed in the United States. Pest Control 39:13-14. Kimura, Y., and K. Nakazawa. 1973. Local variations of susceptibility to organophosphorus in- secticides in the green rice leafhopper in Hiroshima prefecture. Chugoku Agric. Res. 47:100- 102. LeBaron, H. M. 1984. Principles, problems, and potentials of plant resistance. Pp. 351-356 in Biosynthesis of the Photosynthetic Apparatus, J. P. Thornberg, L. A. Staehelin, and R. B. Hallick, eds. New York: Alan R. Liss. LeBaron, H. M., and J. Gressel, eds. 1982. Herbicide Resistance in Plants. New York: John Wiley and Sons. Liu, M-Y., Y-J. Tzeng, and C-N. Sun. 1981. Diamondback moth resistance to several synthetic pyretRroids. J. Econ. Entomol. 74:393-396. Magee, P. S., G. K. Kohn, and J. J. Menn, eds. 1984. Pesticide Synthesis through Rational Approaches. Washington, D.C.: American Chemical Society. Malcolm, C. A. 1983. The genetic basis of pyrethroid and DDT resistance interrelationships in Aedes aegypti. II. Allelism of RDDT2 and Rpy Genetica 60:221-229. Martin, H., and C. R. Worthing, eds. 1977. Pesticide Manual. Basic Information on the Chemicals Used as Active Components of Pesticides. 5th ed. Croydon, England: British Crop Protection Council. Martinez-Carrillo, J. L., and H. T. Reynolds. 1983. Dosage-mortality studies with pyrethroids and other insecticides on the tobacco budworm from the Imperial Valley, California. J. Econ. Entomol. 76:983-986. Menn, J. J. 1980. Contemporary frontiers in chemical pesticide research. J. Agric. Food Chem. 28:2-8. 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. Miller, T. A., V. L. Salgado, and S. N. Irving. 1983. The kdr factor in pyrethroid resistance. Pp. 353-366 in Pest Resistance to Pesticides, G. P. Georghiou and T. Saito, eds. New York: Plenum. Muir, R. C. 1979. Insecticide resistance in damson-hop aphid, Phorodon humuli in commercial hop gardens in Kent. Ann. Appl. Biol. 92:1-9. Mullison, W. 1976. The cost of developing pesticides. Down Earth 32(2):34-36. National Research Council. 1951. Conference on Insecticide Resistance and Insect Physiology. Washington, D.C.: National Academy of Sciences. Nolan, J. 1981. Current developments in resistance to amidine and pyrethroid tickicides in Australia. Pp. 109-114 in Tick Biology and Control, Tick Research Unit, G. B. Whitehead and J. D. Gibson, eds. Grahamstown, S. Africa: Tick Research Unit. Nolan, J., W. R. Roulston, and R. H. Wharton. 1977. Resistance to synthetic pyrethroids in a DDT-resistant strain of Boophilus microplus. Pestic. Sci. 8:484-486.
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42 INTRODUCTION Ogawa, J. M., J. D. Gilpatrick, and L. Chiarappa. 1977. Review of plant pathogens resistant to fungicides and bactericides. FAG Plant Prot. Bull. 25:97-111. Ogawa, J. M., B. T. Manji, C. R. Heaton, J. Petrie, and R. M. Sonada. 1983. Methods for detecting and monitoring the resistance of plant pathogens to chemicals. Pp. 117-162 in Pest Resistance to Pesticides, G. P. Georghiou and T. Saito, eds. New York: Plenum. Omer, S. M., G. P. Georghiou, and S. N. Irving. 1980. DDT/pyrethroid resistance interrelationships in Anopheles stephensi. Mosq. News 40:200-209. Parrella, M. P. 1983. Evaluation of selected insecticides for control of permethrin-resistant Liriomyza trifolii on chrysanthemum. J. Econ. Entomol. 76:1460~1464. Patton, S., I. A. Craig, and G. R. Conway. 1982. The pesticide industry. Pp. 61-76 in Pesticide Resistance and World Food Production, G. Conway, ed. London: Imperial College, Mineral Resources Engineering Department. Pimentel, D., D. Andow, R. Dyson-Hudson, D. Gallahan, S. Jacobson, M. Irish, S. Kroop, A. Moss, I. Schreiner, M. Shepard, T. Thompson, and B. Vinzant. 1980. Environmental and social costs of pesticides: A preliminary assessment. Oikos 34:126-140. Pimentel, D., D. Andow, D. Gallahan, I. Schreiner, T. Thompson, R. Dyson-Hudson, S. Jacobson, M. Irish, S. Kroop, A. Moss, M. Shepard, and B. Vinzant. 1979. Pesticides: Environmental and social costs. Pp. 99-158 in Pest Control: Cultural and Environmental Aspects, D. Pimentel and J. H. Perkind, eds. Boulder, Colo.: Westview. Priester, T. M., and G. P. Georghiou. 1980. Cross-resistance spectrum in pyrethroid-resistant Culex quinquefasciatus. Pestic. Sci. 11 :617-664. Quisenberry, S. S., L. A. Lockwood, R. L. Byford, H. K. Wilson, and T. C. Sparks. 1984. Pyrethroid resistance in the horn fly, Haematobia irritans (L.) (Diptera: Muscidae). J. Econ. Entomol. 77:1095-1098. Radosevich, S. R. 1983. Herbicide resistance in higher plants. Pp. 453-479 in Pest Resistance to Pesticides, G. P. Georghiou and T. Saito, eds. New York: Plenum. Roulston, W. J., R. H. Wharton, J. Nolan, J. D. Kerr, J. T. Wilson, P. G. Thompson, and M. Schotz. 1981. A survey for resistance in cattle ticks to acaricides. Aust. Vet. J. 57:362-371. Ryan, G. F. 1970. Resistance of common groundsel to simazine and atrazine. Weed Sci. 18:614- 616. Sawicki, R. M., and A. D. Rice. 1978. Response of susceptible and resistant aphids Myzus persicae (Sulz.) to insecticides in leaf-dip bioassays. Pestic. Sci. 9:513-516. Sawicki, R. M., A. L. Devonshire, A. D. Rice, G. D. Moores, S. M. Petzing, and A. Cameron. 1978. The detection and distribution of organophosphorus and carbamate insecticide-resistant Myzus persicae (Sulz.) in Britain in 1976. Pestic. Sci. 9:189-201. Sawicki, R. M., A. W. Farnham, I. Denholm, and K. O'Dell. 1981. Housefly resistance to pyr- ethroids in the vicinity of Harpenden. Pp. 609-616 in Proc. Br. Crop Prot. Conf.: Pests and Diseases, Vol. 2. Croydon, England: British Crop Protection Council. Schmidt, D. C., S. E. Kunz, H. D. Petersen, and J. L. Robertson. 1985. Resistance of horn flies (Diptera: Muscidae) to permethrin and fenvalerate. J. Econ. Entomol. 78:402-406. Schnitzerling, H. J., P. J. Noble, A. Macqueen, and R. J. Dunham. 1982. Resistance of the buffalo fly, Haematobia irritans exigua (DeMeijere), to two synthetic pyrethroids and DDT. J. Aust. Entomol. Soc. 21:77-80. Sinegre, G. 1984. La resistance des dipteres culicides en France. Pp. 47-58 in Colloque sur la Reduction d'Efficacite des Traitements Insecticides et Acaricides et Problemes de Resistance. Paris: Societe Frangaise de Phytiatrie et de Phytopharmacie.
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MAGNITUDE OF THE RESONANCE PROBLEM ~3 Smirnova, A. $., Ma I. Levi, M. V. Niyazova, E. I. Kapanadze, A. I. Brom~oerg, V, I. Zagroba, A. A. Budylina' R. M, K~znetsova, A. M. I~autsin, and I. A. Kurkina. 1979. Resistance of some common cockroach Blatella germ~ica subpopulat-ions to neopynamin and other insecticides. Med. Parazi~l. Parazit. Bolezni. 48:60-66. Steiner' H. 1973. Cost-benefit analyses in orchards where integrated control is practiced. Eur. and Mediterr, Plant Prot. (3rg. Bull. 3:27-36. Sudderuddin, K. I., and P-F. Kok, 1978. Insecticide resistance in Plutella xylostella collected from the Cameron Highlands of Malaysia. FAO Plant Prot. Bull. 26,53-57. Wards, L. R., G. A. Lewis, and A. NY. Jackson. In press. Pesticide resistance in glasshouse whitefly, Trialeur~des vaporariorum. Res. and Dev. Agric. 2. We-rsmann, R. 1947. Differences in susceptibility to ODT of flies from Sweden and Switzerland. Mitt, Schweiz. Entomol, Cies. ~:484-504. Wood, K. A., B. lI. Wilson, and J. B. Graves. 1981. Influence of host plant on the susceptibility of the fall armyworm to insecticides, J. Econ. Entomol. 74;96-98. World Health Organization. 1976. Resistance of vectors and reservoirs of disease to pesticides. 22nd Rep. WlIO Exp. Comm, Ins~tic. ~N.H.O. Tech. Rep. No. 585. World Health Organization. 1980. Resistance of vectors of disease to pesticides. 5th Rep. WHO Exp. Comm, Ycetor Bm1. Control. W.H.O. Tech. Rep. No. 655. Worthing, C. R., ed, 1979. Pesticide Manual, Croydon, England: British Crop Protection Council. Wright, J. TV., R. E;. Fritz, and J. Haworth. 1972. Changing concepts of vector control in malaria eradication. Annul Rev, Entomol. 17:75-102.
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Representative terms from entire chapter: