-
Intraspecific Variation in Levels of Pesticide Resistance
InField Populations of a Parasitoid, Aphytis melinus
(Hymenoptera: Aphelinidae): The Role ofPast Selection
Pressures
JAY A. ROSENHEIM ANDMARJORIE A. HOY
Department of Entomological Sciences, University of
California,Berkeley, California 94720
FORUM:J. Econ.Entomol.79: 1161-1173 (1986)ABSTRACT Thirteen
populations of Aphytis melinus DeBach, a key biological
controlagent of California red scale, Aonidie/la aurantii
(Maskell),were collected from the citrus-growing regions of
California. Each population's history of exposure to insecticides
wasestimated by determining history of insecticide use at both
local (in-grove) and regional(county-wide) geographical scales.
Concentration/mortality regressions for five insecticideswidely
used in citrus were estimated for the populations. For each
chemical, substantialvariability existed in the responsesof
different populations. LC",,'swere correlated with bothin-grove and
county-wide pesticide use histories; patterns of variability were
best explainedby results of a multiple regression analysis that
combined the influencesof these two histories.Roles of food
limitation, migration, and host distribution in determining
patterns and ratesof evolution of pesticide resistance in arthropod
biological control agents are discussed.
KEY WORDS Aonidie/la aurantii, Aphytis melinus, biological
control, citrus, integratedpest management, intraspecific
variation, pesticide resistance
PRACTITIONERSOF integrated pest management(IPM) in agricultural
cropping systems may em-ploy a diverse array of tactics to control
noxiousorganisms. Many of these tactics may be groupedunder the
categories of biological control, chemi-cal control, cultural
control, and plant resistance.Most of these approaches are
compatible; thus, bi-ological control, cultural control, and the
use ofplant resistance may, with certain noteworthy ex-ceptions
(e.g., Campbell & Duffey 1979, Herzog& Funderburk 1985), be
combined to good effect,as may chemical control, cultural control,
and plantresistance. This mutual compatibility does not,however,
often extend to biological and chemicalcontrol.
The application of broad-spectrum insecticidesfrequently
disrupts the action of arthropod biolog-ical control agents, with
resulting pest resurgencesand secondary pest outbreaks (Bartlett
1964,De Bach 1974) (Fig. 1). This disruption may be dueeither to a
direct toxic effect on predators andparasitoids, whose
susceptibility to insecticides isoften greater than that of the
associated pest species(Croft & Brown 1975), or to an indirect
effect viastarvation, emigration, or lack of hosts after
thereduction of the pest population by the pesticide(Huffaker 1971,
Newsom 1974, Powell et al. 1985)(Fig. 1). This incompatibility
represents a serioushandicap in the development of sound IPM
pro-grams.
Attempts to overcome this handicap have takenseveral forms. One
is the use of chemicals in an
ecologically selective manner (Hull & Beers 1985).Another is
the use of materials with a physiologicalselectivity based upon
either natural tolerance orevolved resistance of the biological
control agent(Mullin & Croft 1985). The evolution of
resistancein beneficial arthropods through natural selectionin the
field and artificial selection in the laboratoryhas recently been
documented, and such resistantnatural enemies have been
successfully incorpo-rated into IPM programs (Croft & Strickler
1983,Hoy 1985a).
Aphytis melinus DeBach is the major biologicalcontrol agent of
the California red scale, Aonid-iella aurantii (Maskell), in
California and in manyother citrus-growing regions of the world
(Rosen& DeBach 1979), Although the degree of controlexerted by
A. melinus ranges from partial to com-plete in the different
citrus-growing regions ofCalifornia, its effectiveness in all these
regions isseverely impeded by the use of insecticides(DeBach et al.
1971, Bellows et al. 1985, Griffithset al. 1985). Chemicals
commonly applied for con-trol of A. aurantii and other key pests of
citrus notunder biological control, including the citrus
thrips,Scirtothrips citri (Moulton), and several lepidop-teran
species, are toxic to A. melinus (Universityof California,
Statewide IPM Project 1984; Morse& Bellows 1986), resulting in
the destruction ofresident populations and hindering programs
ofaugmentative releases of insectary-reared parasit-oids.
Our study was done to investigate whether A.
1161
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1162 FORUM: JOURNAL OF ECONOMIC ENTOMOLOGY Yol. 79, no. 5
TYPE OFARTHROPODPOPULATION
I Pesticide is ecologically I II selective to population,
IPROXIMATE EFFECTI121; population is naturally I OF PESTICIDE II
tolerant, Q[ population I APPllCA TION IIhas evolved resistance. I
I
Ul TIMA TE EFFECTSOF PESTICIDE APPLICATION
A)I TARGET PEST ~ DEATH 1----~.-11.Suppression of target pest
population. I
Continued biological control.
Probable outbreak of secondary pesl. I
2. Possible resurgence of secondary pest.
3. Collapse 01 biological control agentpopulation due to lack of
hosts or prey(i.e. food limitation, assuming noalternate
hosts).Possible resurgence 01 secondary pesl.
DEATH
DEATH
SURVIVAL" 't-" /\',.1...../ '-~\'~'-'+I4./ "/ ...-----: .
---+15.SURVIVAL
C) BIOLOGICALCONTROL AGENT
B) SECONDARY PEST(Host/Prey of (C
!/ Only pesticides thet ere ellectlve In killing the target pest
are employed, hence the,e Is no yes option. (Some IPMprograms do,
howeve" use allective chemicals at 'ates Intanded to kill only a
p,oportion 01 the target peat populetion.)
Fig. 1. Some proximate .and ~ltimate effects of pesticide
applications on the ecology of arthropod parasitoidjhost and
predator jprey relatIonshIps:secondary pest resurgences and
outbreaks due to the direct effects of pesticidetoxicity and t~e
indirect effects ?f food limitation on biological control agents.
(For purposes of explanation, wepresent scenanos ~here
populat.lOnsshow either 100% mortality or 100% survival; these
outcomes represent thetwo ends of a contmuum of
pOSSibleresponses.Outcomes that are intermediate to both the
proximate and ultimateeffects listed may occur.)
melinus has evolved increased levels of resistancein response to
the selective pressures exerted bythe use of insecticides. We
determined if variabil-ity existed in the resistance levels of
different fieldpopulations of A. melinus, and ascertained if
arelationship existed between these resistance levelsand the
previous insecticide use in the localitieswhere the colonies were
collected. Finally, weconsidered the roles of food limitation,
migration,and host distribution in determining patterns andrates of
the evolution of pesticide resistance in A.melinus.
Materials and Methods
Colony Collection and Maintenance. In Octo-ber 1984, 11
populations of A. melinus were col-lected from the major
citrus-growing regions ofCalifornia (Fig. 2) by two techniques: I)
citrusfruits bearing parasitized A. aurantii were col-lected, and
2) trap fruits (lemons infested with A.aurantii in the laboratory)
were placed in citrustrees to elicit oviposition by A. melinus.
Both tech-niques were used at each collection site. In siteswith
heavy infestations of A. aurantii, the collec-tion of scale-bearing
citrus fruits generally yieldedthe greater number of parasitoids,
whereas in siteswith light infestations use of the trap fruits
wasthe more effective approach. The number of field-collected
parasitoids used to initiate each colonyvaried from 42 to 1,560
(average = 415). The
number of generations (ca. 0-4) required for pop-ulations to
adapt to laboratory conditions and at-tain a normal rate of
increase varied. During thisperiod of adaptation the effective
population sizemay have been substantially less than the total
adultpopulation. In addition to the 11 colonies collectedas
described above, 2 colonies, 1 collected inVentura County in
February 1983 (population 10),and the other a long-term laboratory
colony (pop-ulation 13), were provided by T. S. Bellows andR. F.
Luck (Division of Biological Control, Uni-versity of California,
Riverside), respectively, fortesting. Voucher specimens from each
colony wereconfirmed as A. melinus by D. Rosen, HebrewUniversity,
Rehovot, Israel.
Colonies were maintained in the laboratory at26 2C, 70 10% RH,
and a photoperiod of16:8 (L:D) on a uniparental strain of oleander
scale,Aspidiotus nerii Bouche, that was grown at 24 1C on pink
banana squash, Cucurbita maximaDuchesne, under constant darkness.
This reaTingtechnique was adapted from that described byDeBach
& White (1960). Undiluted honey wasprovided in cages as a
carbohydrate source for A.melinus.
Bioassays. Adult male and female A. melinus(0-48 h old) were
collected for testing with pes-ticides by placing squash bearing
parasitized scalein an emergence cage similar to that described
byAbdelrahman (1973). The cage consisted of a sealedplastic garbage
can with 12 holes drilled in the
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October 1986 ROSENHEIM& Hoy: PESTICIDERESISTANCEVARIATIONIN
A. melinus 1163
Fig. 2. Distribution of commercial citrus in Cali-fornia. Each
dot represents 405 ha. Numbered circlesare collection sites for A.
melinus colonies.
cover. Each of these holes was filled with a glasstest-tube (12
by 75 mm) containing streaks of hon-ey. By illuminating from above,
we then drew theparasitoids, which are positively phototropic
andnegatively geotropic, into the tubes, where theywere harvested.
Cages were emptied and cleanedevery 48 h to provide parasitoids
that were 0-48hold.
Concentration/mortality data were generated byconfining between
10 and 20 adult parasitoids ina treated disposable plastic cup (30
ml) cappedwith untreated polyester gauze upon which undi-luted
honey was provided. The cups were treatedby dipping them for 5 s
into insecticide solutionsformulated in distilled water with a
spreader (0.1%Triton AG-98). Cups were drained onto papertoweling
and air dried. Three materials widely usedfor California red scale
control (carbaryl [Sevin 80sprayable], malathion [Malathion 25
spray able], andmethidathion [Supracide 2 emulsifiable
concen-trate]), one material used for thrips control (di-methoate
[Cygon 400]), and one material used forcontrol of both California
red scale and a complexof lepidopterous pests (chlorpyrifos
[Lorsban 4emulsifiable concentrate]) were tested.
At least five concentrations and a water / spread-er control
were tested for each chemical. Vials wereheld at 26 1C, 87% RH, and
a 16:8 photoperiodfor 24 h before the tests were scored.
Individualswere considered dead if they were unable to main-tain a
normal posture or walk normally, coveringat least 1 mm/s. With a
given chemical, all pop-ulations were tested simultaneously. Each
test was
repeated on at least three different days for a totalof 4-18
replicates per concentration.
Data were analyzed by probit analysis with thePOLO computer
program (Russell et al. 1977).Hypotheses of parallelism (equal
slopes) andequality (equal slopes and intercepts) were testedwith
likelihood-ratio tests (Savin et al. 1977). Pop-ulations were
considered to have different toler-ances if the hypothesis of
equality was rejected(a= 0.05).
Pesticide Use Histories. To investigate the re-lationship of
past exposure to insecticides to ob-served population resistance
levels, we investigat-ed each population's history of insecticide
exposure.(Population 13, a laboratory colony, was not in-cluded in
this analysis.) This was done indirectlyby assessing 1) the past
use of insecticides in thegrove from which the colony was collected
(thelocal or in-grove pesticide use) during the 5-yearperiod
(1980-84) and 2) the past use of insecticidesin citrus groves in
the surrounding areas (the re-gional or county-wide pesticide use)
for the sameperiod.
In-grove and county-wide pesticide use historieswere obtained
from individual growers and theCalifornia Department of Food and
Agriculture,Division of Pest Management (unpublished rec-ords,
Sacramento, Calif.), respectively. We as-sumed that results of
these 5-year surveys wouldapproximate the relative overall levels
of historicalpesticide use not only for 1980-84, but for an
ear-lier period of time as well, during which A. meli-nus was
present in California; the groves sampledwere mature and had been
under single ownershipfor more than the 5-year period surveyed.
Also,patterns of pesticide use were consistent over timein those
groves for which more extensive historieswere available.
The influences of in-grove and county-wide pes-ticide use were
evaluated both independently andin combination using bivariate (one
independentvariable) and multiple (two independent vari-ables)
regression analysis from the SPSS' computerstatistical package
(SPSS 1986, 662-686). Forregressions involving tolerances to
organophospho-rus (OP) insecticides, the local and regional
histo-ries of total OP use were the independent vari-ables. For
regressions involving tolerances tocarbaryl, the corresponding
histories of carbamateinsecticide use were used. Insecticides of
the sameclass (OP or carbamate) were combined in thismanner in an
attempt to include the possible ef-fects of cross-resistance.
An index of overall resistance of each colonywas calculated
relative to that of colony 1. Eachcolony's LC50 for an insecticide
was divided bythat of colony 1. A similar ratio was calculated
foreach of the insecticides for which the colony wastested, and the
ratios were totaled and averagedfor each colony. The resulting
overall average rel-ative resistance values were then regressed
againstthe total number of insecticide treatments applied
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1164 FORUM: JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 79, no. 5
to the grove from which the colony came, againstthe county-wide
pesticide use, and against thecombined level of in-grove and
county-wide pes-ticide use.
Finally, for each chemical tested, we deter-mined whether the
slope values of the concentra-tion/mortality regressions were
linearly related to1) the associated LCoo's, 2) the selective
pressureexperienced by the population (as estimated bythe sum total
of the in-grove and county-wide pes-ticide use histories), or 3)
the degree to which thelevel of in-grove pesticide use diverged
from thatof the county (as estimated by subtracting the in-grove
pesticide use value from the county-widepesticide use value).
Results
For each of the five insecticides tested, the
con-centration/mortality regressions varied signifi-cantly among
the A. melinus colonies (Table 1).The hypothesis of equality was
rejected for mostpopulation comparisons for each chemical.
The collection site characteristics and the in-grove and
county-wide pesticide use histories forthe 13 colonies tested are
shown in Table 2. Allbut two of the collection sites were
commercialgroves. The species of Citrus chosen was generallythe one
that was predominantly grown in the re-gion being sampled. The
overall amounts of insec-ticides used varied widely, both
regionally amongcounties (0.099-4.67 kg [AI]/ha per year), and
lo-cally among groves (0-15 applications from 1980to 1984). No
significant relationship between thetotal (carbamate plus OP)
in-grove and county-wide insecticide use was found (r2 = 0.0012; P
>0.25). Since A. melinus colonies were collectedfrom groves that
were chosen for their varied his-tories of pesticide use, a lack of
correlation wasexpected.
The results of the regression analyses of the LCso's(Table 1) on
the levels of past pesticide use (Table2) are shown in Table 3. The
slopes of the signif-icant regressions were all positive,
indicating apositive correlation between LCso's and levels ofpast
pesticide use. Due in part to the small samplesize (7-11), the
levels of significance associated withthe single independent
variable correlations wereoften inadequate to draw strong
conclusions. (Forthe eight nonsignificant regressions, 0.14 ~ P
~0.44.) However, when the influences of the twofactors, the
in-grove and county-wide pesticide usehistories, were combined, the
resulting regressionswere strong enough to be significant for three
ofthe five chemicals tested (P ~ 0.10). (Due to thesmall sample
sizes employed, a = 0.10 was used.Additional studies with larger
sample sizes will benecessary to confirm these results and reduce
theoverall risk of type I error.) This suggests that boththe
in-grove and county-wide pesticide use are im-portant in accurately
describing a population's his-tory of selection pressures.
Table 1. Variation in concentration/mortality regres-sions of A.
melinu. colonies collected from California ex-posed to residues of
five insecticides
Insec- Col- nO SI SEM LCso (95% CL)!icide ony ope in mg
(AI)/liter
Carbaryl (suggested field rateb: 960 mg [All/liter)7 1,182 3.22
0.20 15.4 (13.3-17.5)a8 1,061 3.42 0.22 17.9 (l5.8-20.1)b5 1,101
3.91 0.24 19.9 (l8.5-21.4)c
1I 1,153 3.74 0.21 19.9 (18.1-21.8)cd4 983 4.27 0.25 23.5
(21.5-25.9)e3 498 3.10 0.30 24.0 (20.3-28.2)f1 648 4.28 0.42 27.9
(24.4-31.2)g
Chlorpyrifos (suggested field rate: 450 mg [All/liter)7 427 2.70
0.26 0.78 (0.58-0.97)a
1I 1,337 3.31 0.16 0.84 (0.76-0. 92)ab3 1,443 2.55 0.14 0.93
(0.81-1.06)c4 381 3.40 0.32 1.02 (0.87-1.20)d5 1,035 3.59 0.27 1.11
(0.98-1.23)de8 614 5.69 0.78 1.24 (1.01-1.40)f1 1,172 4.60 0.51
1.37 (1.l8-1.50)g2 255 2.42 0.33 1.43 (1.06-2.07)h
Dlmelhoale (suggested field rate: 1,200 mg [All/liter)9 325 3.06
0.47 2.18 (1.26-2.85)a7 1,444 2.69 0.15 2.58 (2.19-2.96)b
13 410 3.09 0.29 2.73 (2.25-3.20)bc10 1,168 2.28 0.13 2.73
(2.33-3. 15)d3 1,143 2.63 0.15 3.55 (3.02-4. 13)e2 438 2.65 0.29
3.62 (2.64-4.62)ef8 1,464 2.55 0.13 3.91 (3.40-4.46)ef
12 196 2.70 0.37 3.95 (2.82-5.79)efg6 910 2.71 0.17 4.16
(3.57-4.79)fg4 1,244 2.72 0.17 4.46 (3.75-5.25)g1 435 2.67 0.49
6.36 (3.49-8.71)h
Malathion (suggested field rate: 720 mg [All/liter)9 929 2.65
0.15 0.54 (0.45-0.63)a
13 460 3.15 0.24 0.78 (0.57-0.99)b7 1,436 2.78 0.13 1.23
(1.09-1.37)c
10 1,521 3.20 0.19 1.27 (1.l0-1.42)cd6 1,369 2.50 0.14 1.73
(1.50-1.98)e
12 1,226 4.52 0.35 1.94 (1.72-2.15)f3 1,644 3.09 0.20 2.07
(1.84-2.28)g8 1,459 3.56 0.25 2.29 (1.99-2.57)hc
1I 869 4.43 0.31 2.36 (2.07-2.67)h2 1,294 2.98 0.24 2.37
(2.02-2.70)h4 1,272 3.04 0.15 3.1I (2.69-3.58)i1 553 2.53 0.31 4.22
(3.33-5. 16)j
Methidathion (suggested field rate: 300 mg [All/liter)9 1,102
2.38 0.14 0.44 (0.37-0.51)a6 1,093 2.43 0.16 2.07 (1.79-2.37)b8
1,121 2.45 0.15 2.30 (2.03-2.60)bc1 957 2.90 0.22 2.46
(2.13-2.81)cd5 776 2.80 0.24 2.54 (2.19-2.97)cd2 1,231 2.08 0.17
2.68 (2.16-3.23)&3 1,055 2.57 0.17 2.71 (2.32-3.15)de4 654 2.30
0.20 3.00 (2.54-3.58)e
12 286 1.99 0.36 3.36 (1.76-7.90)e
Concentration/mortality regressions followed by the same let-ter
are not significantly different (a = 0.05; likelihood-ratio
test[Savin et al. 1977]).
o Natural mortality ranged from 0 to 8.8 1.9% and
averaged2.2%.
b Recommendations of the University of California
CooperativeExtension citrus treatment guide (Morse & Bailey
1984).
c The regression for colony 8 is not significantly different (a
=0.05) from the regressions of colonies 1I or 2. However,
theregression of colony 1I is significantly different from that of
col-on12.
The regression for colony 1 is not significantly different (a
=0.05) from the regressions of colonies 5 or 3; likewise, the
regres-sion for colony 3 is not significantly different from that
of colony2. However, the regression for colony 2 is significantly
differentfrom those of colonies 1 and 5.
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October 1986 ROSENHEIM & Hoy: PESTICIDE RESISTANCE VARIATION
IN A. melinus 1165
t-
o
o
oo
o
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1166 FORUM: JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 79, no. 5
c.9'5.D'1:
""0lI:l .000
."""go+1
." 0.10). Fig. 3C shows the expected values ofeach colony's
overall average relative tolerance, aspredicted by the multiple
regression equation, ver-sus the observed values of the same.
Linear regression analysis showed that the slopesof the
concentration/mortality regressions were notcorrelated with either
the associated LC50's, thetotal pesticide use history, or the
difference be-tween the in-grove and county-wide pesticide
usehistories. The slopes of the regression lines variedfrom
positive to negative for different chemicals,and the correlations
were generally not significant(data not shown). The fact that the
slopes of theprobit regressions were not positively correlatedwith
their LCw's indicates that the intrapopulationvariation in
resistance (i.e., change in response perunit increase of
concentration) has not decreasedas the LCso's have increased in
response to selec-tion pressures. This suggests that additional
re-sponses to selection could occur.
-
( = 0.372 + 0.024(;n-o,ove use) + 0.066(counly-wide useU
1167
-Fig. 3. Regression analyses of each colony's overallaverage
relative tolerance on (A) its in-grove pesticideuse history, (B)
its county-wide pesticide usehistory, and(C) both A and B
simultaneously (multiple regression).See Table 2 for values
plotted.
1957 to 1960. Approximately 2.5 million insectary-reared
parasitoids were released into 200 citrusplots; these parasitoids
originated from a singleculture consisting of a mixture of four
small col-lections made in Pakistan and India (DeBach 1959,DeBach
& Landi 1959, DeBach & Sundby 1963).Since these initial
introductions, the degree of re-sistance of A. melinus populations
to the insecti-cides tested appears to have diverged. The
mostsusceptible colony tested, colony 9, originated froma
population that has been exposed to insecticidesonly minimally.
This colony's in-grove pesticideuse history is known for the
21-year period, 1964-84, during which only four applications of
broad-spectrum OP insecticides were made. In addition,this
population is relatively isolated from other ex-tensive citrus
plantings, suggesting that migrationof individuals from heavily
sprayed areas into thispopulation may have been relatively low. The
mostresistant colonies had LCso's up to 7.8-fold greaterthan that
of this colony (Table 1). The evolutionof increased resistance to
pesticides by A. melinusappears to represent an example of post
releaseadaptation in a species introduced for classical bi-ological
controL
The evolutionary divergence of A. melinus pop-ulations also
reflects evolutionary flexibility in pop-ulations that might have
been expected to be rel-atively low in genetic variability. A.
melinus is amember of the order Hymenoptera, which hasbeen found to
display the least amount of electro-phoretically detected genetic
variation of any ofthe insect orders (Graur 1985). Although
withinthe Hymenoptera solitary wasps show a greaterlevel of average
heterozygosity than do the socialspecies, they still exhibit less
variation than non-hymenopteran orders (Graur 1985). Furthermore,A.
melinus is a recently introduced species. Thegenetic variability of
species introduced to a newarea as part of a biological control
program maybe reduced by the limited numbers of
individualscollected from the indigenous area, genetic driftand
inadvertent selection during the processes ofquarantine and
mass-rearing, and additional bot-tlenecks occurring during the
release and coloni-zation of the new habitat (Messenger & van
denBosch 1971, Hoy 1985b). It is unknown to whatextent, if any, the
process of importing A. melinushas reduced the evolutionary
flexibility of its Cal-ifornia populations .
Previous ipvestigations of the evolution of resis-tance to
insecticides among field populations ofparasitoids have yielded
mixed results. Adams &Cross (1967) reported no significant
difference be-
1.0
0.6
Y 0.490 + 0.088
,2 0.38
Y 0.548 + 0.025
,2 . 0.28
,2 0.62
0.6
0.4
ROSENHEIM & Hoy: PESTICIDE RESISTANCE VARIATION IN A.
melinus
In-grove peltlclde use history
County-wide pesticide use history
0.2
Combined in-grove and county-wide pesticide use index
1.0 B
"Eu0.'ii!..~~ 0.4'".~.;; ~ 0.2~0
00
1.0 C
oo
~ 0.2
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1168 FORUM: JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 79, no. 5
tween the tolerances of three field and one labo-ratory colony
of Bracan mellitor Say to five insec-ticides used on cotton.
Similarly, Krukierek et al.(1975) failed to detect differences
between the re-sponses to oxydemeton-methyl of two populationsof
Trichagramma evanescens Westwood or twopopulations of T. minutum
Riley. Strawn (1978)was unable to detect significant variation in
theresponses of either adults of four field populationsof
Comperiella bifasciata Howard or pupae of sixpopulations of A.
melinus to four OP compounds.Likewise, no significant differences
in levels of re-sistance to malathion were exhibited by seven
fieldpopulations of Aphytis holoxanthus DeBach(Havron 1983).
In contrast, Schoonees & Giliomee (1982) founda 5.7- and a
65.6-fold difference in levels of resis-tance to methidathion in
two field populations ofAphytis african us Quednau and two field
popu-lations of C. bifasciata, respectively. Strawn (1978)found
significant interpopulation variation in re-sponse to parathion by
C. bifasciata pupae and inthe tolerances of A. melinus adults to
dimethoate,methidathion, and parathion. Unfortunately, be-cause
Strawn's tests were performed using single-dose bioassays and
because probit regressions werenot generated, further comparison of
these resultswith ours is difficult. Finally, Hsieh (1984) founda
ca. 2-fold difference between the tolerances ex-hibited by two
field populations of Diaeretiellarapae (M'Intosh) to methomyl. Thus
the increasein resistance levels exhibited by parasitoids pro-duced
by natural selection in the field has variedfrom undetectable to
substantial. In none of thesestudies, in which explicit comparisons
of differentpopulations were made, was the increased level
ofresistance adequate to enable adult parasitoids tosurvive field
application rates of insecticides. Thepattern of evolution of
resistance among parasit-oids clearly does not resemble the
explosive emer-gence of resistance in pest species (Georghiou
&Mellon 1983).
Several possible explanations for this apparentrelative
inability of parasitoids to develop resis-tance have been proposed.
The evolution of resis-tance in field populations of parasitoids
may oftengo unnoticed (Croft & Brown 1975). The differ-ential
exposures of parasitoids relative to their hostsdue to
morphological, behavioral, or ecological dif-ferences may lead to a
greater effective toxicity(Georghiou 1972). Because parasitoids are
ofteninitially less tolerant of pesticides than their hosts,a
larger increase in tolerance may be required toachieve effective
levels of resistance (J.A.R., un-published data). The lack of
genetic flexibilityamong the highly ecologically specialized
parasit-oids may restrict the evolution of resistance (Huf-faker
1971, Georghiou 1972). The relatively lowactivity of preadapting
detoxifying enzyme sys-tems may limit the potential for resistance
(Croft& Strickler 1983). Finally, the reliance of parasit-oid
populations upon the host population for sur-
vival after pesticide applications may effectivelyselect against
resistant individuals (Croft & Morse1979, Hoy 1979, Tabashnik
& Croft 1985). Thelast hypothesis, the food limitation
hypothesis, hasreceived increased attention recently (Morse
&Croft 1981, Tabashnik & Croft 1982, 1985, Ta-bashnik
1986).
A corollary of the food limitation hypothesis(Georghiou 1972,
Morse & Croft 1981, Croft &Strickler 1983, Tabashnik &
Croft 1985) is thatresistance is unlikely to develop in a natural
enemyspecies until after its host or prey (henceforth calledhost)
has become resistant. Consideration of thepatterns of pesticide use
in citrus and the resultingimpact on A. melinus and its host scale
popula-tions leads to the conclusion, however, that thiscorollary
may have been described in an overlyrestrictive form. Generally,
chemicals being dis-cussed in this regard are not directed against
thehost population. Rather, they are being used tocontrol other key
pests in the agroecosystem.Therefore, resistance in the host
population is notalways necessary; any means by which this
popu-lation can survive the pesticide application andthereby
continue to serve as hosts to the naturalenemy species will
circumvent the problem of foodlimitation.
There are two general means by which a non-resistant host
population can survive an insecticideapplication (Fig. 1). First, a
non-resistant host pop-ulation will be relatively unaffected by a
chemicalapplication that it does not physically contact.
Forexample, dimethoate applied to control citrus thripsis applied
only to the periphery of the tree (Table4). The dimethoate will,
therefore, contact only afraction of the total California red scale
popula-tion, which is distributed throughout the tree(Ebeling
1959). The same is true for chlorpyrifos,which is applied to the
outside of the tree for con-trol of various orangeworms (Table 4).
The appli-cation of pesticides to a restricted portion of thetree
may be described as a form of ecological se-lectivity towards the
host population. Second, anatural tolerance relative to the
tolerance of thetarget pest species will also enable the host
popu-lation to survive treatment. Thus, California redscale, while
potentially controllable with dimeth-oate (which is registered for
control of A. auran-tii), largely appears to be tolerant of the
lowerconcentrations applied for control of citrus thrips.
The results of our study may be considered withregard to this
broadened concept of the food lim-itation hypothesis and its
corollary. The absenceof a substantial host population should,
accordingto the hypothesis, retard the evolution of resistancein A.
melinus to carbaryl, malathion, and methi-da'thion (used to control
scales) but not to dimeth-oate (applied for thrips control). The
evolution ofresistance to chlorpyrifos (applied for control
ofeither scales or orangeworms) should fall some-where between
these two extremes.
Are these predictions reflected in the ranges of
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October 1986 ROSENHEIM& Hoy: PESTICIDERESISTANCEVARIATIONIN
A. melinus 1169
Table 4. Recommendations" of the University of California
Cooperative Extension for the treatment of citrus withcarbaryl,
chlorpyrifos, dimethoate, malathion, and methidathion
Earliest recommendation 1984-86 recommendationPesticide and
Target species Cover- Cover-formulation Year Concn age Concn
age
typei' type
Carbaryl A. auranlii 1966-67 1.20-1.44 g/liter TC Same as
1966-6780WP (1-1.2 Ib/loo gal)
Chlorpyrifos Several Lepidopteran 1984-86 1.24-12.4 ml/liter/ha
OC Same0.48 kg/liter E pests (1-2 qt/l00-5oo gal/acre)(4lb/gal) A.
auranll/ 1984-86 0.94 ml/liter TOC Same
(0.75 pt/loo gal)
Dimethoate S. citri 1966-67 3.75 ml/liter MS 4.64-18.5 mlfliter
OC0.32 kg/liter E (3 pts/loo gal) 3-6 pts/l00-2oo gal/acre"(2.67
Ib/gal)
Malathion A. aurantii 1957d 3.00-4.20 g/liter TC 2.88-4.07
g/liter TC25WP (2.5-3.5 Ib/loo gal) (2.4-3.4 Ib/loo gal)
Methidathion A. auranlii 1976-78 1.25 ml/liter TOC Same as
1976-780.24 kg/liter E (1 pt/loo gal)(2Ib/gal)
U Recommendations published in the irregularly issued citrus
treatment guides (e.g., Morse & Bailey 1984)./,Abbreviations
used are taken verbatim from treatment guides (e.g., Morse &
Bailey 1984). MS, mist spray; low Iiterage, 936-2,807
liters per hectare (100-300 gallons per acre), applications
without droplet size restrictions achieving limited droplet
depositions ontree surfaces; OC, outside coverage; median Iiterage,
not more than 4,676 liters per hectare (500 gallons per acre),
applicationsachieving thorough distribution to outside or
peripheral parts of the tree only; TC, thorough coverage: high
Iiterage, 114-132 litersper tree (30-35 gallons per tree),
applications achieving thorough film wetting of all interior and
exterior parts of the tree; TOC,thorough distribution coverage:
median Iiterage, 76-114 liters per tree (20-30 gallons per tree),
applications achieving thoroughdistribution to all interior and
exterior parts of tree without necessity of obtaining film
wetting.
" For the first time, in the 1984-86 Treatment Guide, this
recommendation was accompanied by a footnote reading
"Non-resistantthrips only."
of Because A. melinus was introduced in 1957, this is the
earliest relevant recommendation.
resistance values observed in the populations testedwith each of
these insecticides? Because not allcolonies were tested with all of
the chemicals, theranges of resistance values must be considered
withcaution. To compare the ranges of resistance val-ues for two
chemicals, only those colonies testedwith both chemicals should be
considered (e.g., tocompare the ranges of LCso's of carbaryl with
di-methoate, only colonies 1, 3, 4, 7, and 8 should beincluded).
The LC50's for these colonies (Table 1)indicate that the maximum
ranges of resistanceare 27.9/15.4 = 1.8-fold for carbaryl and
6.36/2.58 = 2.5-fold for dimethoate. The ranges of re-sistance
values observed for malathion and di-methoate were 7.8- and
2.9-fold, and methidathi-on and dimethoate were 7.7- and 2.9-fold,
respec-tively. Analogous figures for the three scalicides,carbaryl,
malathion, and methidathion, comparedwith chlorpyrifos are 1.8- and
1.7-fold, 3.4- and1.8-fold, and 1.3- and 1.5-fold, respectively.
Thefood limitation hypothesis predicts that the secondvalue of each
of these paired numbers, represent-ing the extent of evolved
resistance to chemicalsnot impacting the host population, should
begreater than the first value, representing the extentof evolved
resistance to chemicals that reduce thehost population. However,
our observations sug-gest the reverse. This is a limited test of
the hy-pothesis; many other factors, including the lengthof time
and the degree to which the chemicalshave been used (Tables 2 and
4) and the possible
existence of cross-resistance patterns, will affect theoutcome.
We conclude that, at least in this system,food limitation does not
appear to be the key fac-tor in determining the extent to which
resistancehas developed.
The Role of Past Selection Pressures. One ofour two initial
goals was to evaluate thp role ofpast selection pressures in any
observed interpop-ulation patterns of variation. To measure
selectionpressures, spatial delimitation of a population
wasrequired. Two important considerations were thegeographic
distribution of potential hosts and thedispersal ability of the
parasitoid.
The distribution of hosts of A. melinus provedto be difficult to
describe. Although the distribu-tion of commercially cultured
citrus in Californiais known to consist of several fairly discrete
regionsin widely separated valleys bounded by substantialmountain
ranges (Fig. 1), we concluded that com-mercial citrus did not
represent the entire hostplant pool. Substantial scale populations
also existin common, small, dooryard citrus plantings(DeBach 1965).
A. aurantii also infests many otherhost plants. McKenzie (1956)
considered the speciesto be one of California's 22 omnivorous
armoredscales, and the total number of plant hosts may belarge
(Quayle 1911, McKenzie 1946). Compound-ing this situation in
California, A. melinus devel-ops not only on A. aurantii but also
on nine otherspecies of armored scales (Rosen & De Bach 1979;S.
C. Warner, personal communication). Most of
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1170 FORUM: JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 79, no. 5
these additional hosts are also omnivorous; Mc-Kenzie (1956)
listed over 80 plant genera, includ-ing many commercially
cultivated species, as "onlya few of the more preferred hosts."
The significance of these alternate hosts is dif-ficult to
assess, and their collective contribution tothe total host pool may
be less than that of A.aurantii (R. F. Luck, personal
communication). A.melinus is not the dominant parasite of any of
thealternate hosts (R. F. Luck & S. C. Warner, per-sonal
communications), and some of the scales arerelatively rare.
However, alternate host scale/hostplant combinations may provide
refugia and av-enues for population movement both within andbetween
the major citrus-growing areas.
Although the dispersal ability of A. melinus hasnot been
investigated specifically, reports of theparasitoid's spread
following introduction into newareas provides a crude estimate of
its mobility.From studying the spread of A. melinus in
Greecefollowing its introduction there, DeBach & Argy-riou
(1967) concluded that its effective rate of dis-persal was 75-100
km per year, even across rela-tively barren land cultivated only in
scattered areas.De Bach & Sundby (1963) noted that A.
melinuscould cross a 15-km barrier of barren high hillsseparating
California's San Fernando and SimiValleys. On a smaller scale, the
ability of the para-sitoid to spread throughout an Australian
citrusgrove within 10 months of its release was docu-mented by
Campbell (1976). Thus, A. melinus ap-pears to have a well-developed
ability to disperse.
The diffuse nature of the host pool of A. meli-nus, coupled with
the parasitoid's mobility, indi-cated that an investigation of both
the history ofpesticide use in the grove where the populationsample
was collected and some measure of pesti-cide use in the surrounding
areas would be nec-essary to adequately describe the historical
selec-tion pressures experienced by the population.Although not
precise and not. explaining all of thevariability in LC~o's of the
populations sampled,the combined influences of these two factors
ap-pear to provide a means of explaining the essentialfeatures of
the observed patterns. Part of the unex-plained variability may
also be attributable to theartificial movement of A. melinus
populations re-sulting from the activities of commercial
insecta-ries and biological control workers.
Unfortunately, it is difficult to compare theseconclusions with
those drawn from other studiesdealing with either beneficial or
pest arthropods.Many authors have hypothesized that either thelocal
history of pesticide use (e.g., Georghiou 1966,Herne 1971, Penman
et al. 1976, Strawn 1978,Hoy & Knop 1979, Schoonees &
Giliomee 1982,Mansour 1984, Quisenberry et al. 1984, Robertson&
Stock 1985, Schmidt et al. 1985, Georghiou1986), regional history
of pesticide use (e.g., Geor-ghiou 1972, Grafton-Cardwell & Hoy
1985), orsome combination of the two (e.g., Follett et al.1985)
have generated patterns of variable resis-
tance observed. Although suggestive data are pre-sented in these
studies, we are not aware of anyinstance in which these hypotheses
have been testedstatistically. Hopefully, future studies will
includeanalyses of 1) past selection pressures, and 2) theroles of
migration and host distribution in affectingthe relative importance
of local and regional pat-terns of pesticide use. Progress in the
nascent fieldof resistance management, which attempts to pro-long
the useful life of pesticides by slowing or halt-ing the evolution
of resistance, is dependent uponthe ability to implement specific
pesticide usestrategies. The results of the studies we
proposeshould be relevant to determining the geographicscale over
which such resistance management pro-grams should be implemented
for optimal effect.
Implications for IPM, The results of this studyare encouraging
because the observed trend to-wards increased resistance levels
indicate a possi-ble means of increasing the effectiveness of
A.melinus within an IPM framework. However, forat least three
reasons, these results are not yet causefor complacency. First,
levels of resistance exhib-ited by the populations sampled were not
sufficientto enable them to survive field application rates
ofcommonly used insecticides. This conclusion is inaccordance with
other recent studies performedboth in the laboratory (Bellows et
al. 1985, Morse& Bellows 1986) and the field (Griffiths et al.
1985).Second, we have no way to predict whether or notthe observed
trend towards increased resistance willcontinue in the future.
Finally, A. melinus doesnot exist in an ecological vacuum. While
popula-tions of this parasitoid may be evolving increasedtolerance
levels, the pest populations against whichthe chemicals are being
applied may simulta-neously be evolving increased resistance.
Growersmay be forced, thereby, to increase their insecti-cide
application rates or shift to the use of newinsecticides. These
responses represent an intensi-fication of old selection pressures
and the creationof new selective pressures upon the parasitoid
pop-ulation. Thus, the parasitoid may be engaged inan evolutionary
race to resistance with the keypests of citrus.
Since the introduction of A. melinus in 1957,California citrus
growers have had relatively fewproblems with resistant insect
pests. For all theinsecticides tested, the recommended
applicationrates have remained essentially unchanged from1957 to
the present (Table 4). A warning regardingresistant populations
does, however, accompany therecommended application rates for
dimethoate forthrips control. The citrus thrips is the only
keyinsect pest of citrus that has recently developedresistance to
an insecticide widely used for its con-trol (Morse & Brawner
1986). The declining effec-tiveness of dimethoate is reflected in
the increasingapplication rates used by some growers. Fig. 4
pro-vides one such example taken from a grove in ButteCounty.
Within the last few years, many growershave begun using
insecticides other than dimeth-
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October 1986 ROSENHEIM & Hoy: PESTICIDE RESISTANCE VARIATION
TN A. melinus 1171
Fig. 4. Dimethoate application rates for citrus thripscontrol in
a Butte County navel orange grove, 1967-84.
Acknowledgment
We thank the many Univ. of California CooperativeExtension
entomologists and California citrus growerswho assisted with the
collection of parasitoids and pro-vided pesticide use histories.
Special thanks go to J. Gor-den and J. R. Stewart (Pest Management
Associates, Ex-eter, Calif.), T. S. Bellows, R. F. Luck, and S. C.
Warner(Univ. of California, Riverside), R. Frinfrock (FAR
Inc.,Corona, Calif.), D. J. Sandri and T. G. Shanower (Univ.of
California, Berkeley), J. L. Robertson (Pacific South-west Forest
and Range Exp. Stn., U.S. Forest Service),and D. Rosen (Hebrew
Univ., Rehovot, Israel). We thankL. E. Caltagirone, G. Thomson, and
R. F. Luck for crit-ical reviews of the manuscript. We also thank
the Amer-ican Cyanamid, CIBA-Geigy, Dow Chemical, and UnionCarbide
corporations for providing insecticides for test-ing. This material
is based upon work supported in partby USDA Competitive Grant
#84-CRCR-I-1452, Re-gional Research Project W-84, and under a
NationalScience Foundation Graduate Fellowship to J.A.R.
oate for thrips control. Thus, A. melinus may al-ready have
missed the opportunity to become re-sistant to dimethoate. The
other insecticides testedin this study continue to be used, but
further in-creases in the resistance levels exhibited by A. mel-in
us will be necessary before they can be usedselectively.
One means to obtain these additional increasesin resistance is
through a program of artificial se-lection in the laboratory.
Artificial selection hasbeen successful in producing populations of
pred-ator mites (Roush & Hoy 1981, Hoy 1985a) and apredaceous
insect (Grafton-Cardwell & Hoy 1986)that are able to survive
exposure to field concen-trations of insecticides. Thus far,
selection of insectparasitoids has been unsuccessful. Based upon
ourobservations of increased resistance levels in pop-ulations of
A. melinus and the retention of intra-population variation in
resistance levels in thesepopulations, A. melinus appears to be an
appro-priate subject for a program of artificial selection.
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