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OCR for page 14
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
OCR for page 15
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.
OCR for page 16
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.
OCR for page 17
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
OCR for page 18
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.
OCR for page 19
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OCR for page 20
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
OCR for page 21
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
OCR for page 22
22
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OCR for page 23
23
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OCR for page 24
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
OCR for page 34
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.
OCR for page 35
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).
OCR for page 36
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
OCR for page 37
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.
OCR for page 38
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.
OCR for page 39
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.
OCR for page 40
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
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Representative terms from entire chapter:
potato beetle
