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Carbamate and Pyrethroid Resistance in the Leafminer
J. A. ROSENHEIM,' AND B. E. T ABASHNIK Department of Entomology, University of Hawaii at Manoa, Honolulu, Hawaii 96822 J. Econ.Entomol.83(6): 2153-2158 (1990) ABSTRACT Populations of D1glyphus begini (Ashmead), a parasitoid of Lirlomyza leafminers, showed resistance to oxamyl, methomyl, fenvalerate, and permethrin in labo-ratory bioassays. Relative to a susceptible strain from California, maximum resistance ratiosfor these pesticides were 20, 21, 17, and 13, respectively. Three populations that had beentreated frequently with insecticides were significantly more resistant to all four insecticidescompared with an untreated Hawaii population and a California population with an unknownspray history. Parasitoids from a heavily sprayed tomato greenhouse on the island of Hawaiihad LC",'s for permethrin and fenvalerate that were 10 and 29 times higher than the fieldrate, respectively. Populations resistant to oxamyl and methomyl had LC",'s two- and sixfoldbelow the field rate, respectively. D. begini is one of the few parasitoids resistant to pyre-throids, with LC",'s exceeding field application rates. Resistant D. begini may be useful forcontrolling leafminers in management programs that integrate biological and chemical con-trols.
Insecta, IPM, pesticide resistance, Lirlomyza INSECTICIDERESISTANCEin beneficial arthropods et al. 1985) and decimation of effective natural with resistance in pests (Croft & enemies (Oatman 1959; Johnson et al. 1980a,b; Ma- Strickler 1983, Georghiou 1986, Croft 1990, Hoy son et al. 1987).
in press, Tabashnik & Johnson in press). Based on In a previous study, five species of parasitic Hy- survey results, Georghiou menoptera associated with L. sativae and L. trifolii for <3% of the 447 in Hawaii were tested to determine their tolerances species of insects and mites known to be resistant to one or more pesticides.
Few hymenopterous 1988). The eulophid Diglyphus begini (Ashmead), parasitoids are resistant to insecticides (Croft 1990, which was accidently & Johnson in press).
the early 1900s (Timberlake 1923), and reintro- During the past several years, studies of insec- duced from Mexico in 1976 (Funasaki et al. 1988), ticide resistance in leaf miners in the genus Lirio- had higher LCso's to both pyrethroids myza (Diptera: Agromyzidae) (Mason et al. 1987, reported earlier for L. trifolii and L. sativae (Ma- 1989) and their hymenopterous parasitoids (Mason son et al. 1987). These results were consistent with & Johnson 1988) have been conducted a study that showed D. begini survived spray treat- The leafminers Liriomyza sativae Blanchard L. trifolii (Burgess) are major pests of tomatoes, 1981). In Florida, a related species, Di- (Girsault) (Eulophidae), 1978, Hara 1986, Johnson 1987) and highly tolerant to fen valerate in laboratory bioas- the world (Parrella 1987). Insecticides says of contact toxicity (Waddill commonly used in vegetable and ornamental studies, intraspecific comparisons between parasit- duction in Hawaii and the continental United States oid populations were not made. Therefore, it could include carbamates not be determined resistance in Di- and permethrin).
glyphus spp. was an innate characteristic these pesticides has led to control problems with ural tolerance) or if resistance resulted from selec- L. sativae and L. trifolii tion with pesticides.
of resistance (Parrella et al. 1984, Keil The objectives of our study were to examine in susceptibility and fen valerate in the leaf miner para- sitoid D. begini. LCso's were compared among five lem,P.O. Box12. Rehovot76-100. Israel.
D. begini populations 1990 Entomological Societyof America JOURNAL OF ECONOMIC tance was a function of the history of insecticide colony's pesticide exposure history was not known.
treatment for each population.
Parasitoids used in the bioassays were 2-4 d old(CA) and 1-4 d old (PO, HO, MO, and GH).
Insecticides. Four formulated insecticides were Materials and Methods used: methomyl (Lannate 1.8 EC, Du Pont), oxa- Sources of Parasitoids. Leaves containing mixed my I (Vydate 2.0 EC, Du Pont), permethrin (Am- populations of Liriomyza sativae and L. trifolii bush 2.0 water soluble liquid [L]; ICI Americas, larvae were collected from three locations (PO, Inc., Wilmington, Del.), and fenvalerate (Pydrin HO, and MO) on the island of Oahu, Hawaii, from 2.4 L; Shell, Houston, Tex.).
February to July 1989. Two of these sites, PO and Field rates for methomyl and oxamyl were cal- HO, had previously received weekly pesticide ap- culated as 1,080 and 1,200 mg (AI) per liter, re- plications. PO was at the University of Hawaii Ex- spectively, based upon recommended periment Station farm at Poamoho, Oahu. The HO of 216 (methomyl) and 240 (oxamyl) g (AI)/liter site was a private commercial farm in Hawaii Kai, or 1.0 and 1.1 kg formulated material/ha, Oahu. MO, the third collection site on Oahu, was tively. Field rates for permethrin and fen valerate an isolated organic garden containing tomatoes and were calculated as 240 mg (AI) per liter, based beans in the Manoa Valley near the University of upon recommended label rates of 240 (permethrin) Hawaii. The owner of this property reported that and 288 (fenvalerate) g (AI)/liter or 0.24 kg for- no chemicals had been applied for the past 20 yr.
Leaves infested with Liriomyza spp were also col- Bioassays. The bioassay procedure was similar lected from a heavily sprayed commercial green- to that described by Rosenheim & Hoy (1986).
house (GH) north of Hilo on the island of Hawaii Adult parasitoids anesthetized with CO2 for 30 s during August to October 1989. The GH green- were sorted by sex 24 h before they were exposed house had received 34 pesticide treatments be- to pesticide residue. D. begini females were placed tween December 1988 and May 1989, including in 36-ml clear plastic cups (Anchor Hocking, Min- of fen valerate (Asana XL 0.66 neapolis, Minn.) with a fine camel's-hair brush. The emulsifiable concentrate [EC]; E. I. du Pont de cups were covered with an organdy square and Nemours & Company, Wilmington, Del.), 11 ap- capped with a plastic lid, the center portion re- plications of methomyl (Lannate 1.8 EC; Du Pont), moved. All insects were kept in an environmental and 7 applications of oxamyl (Vydate 2.0 EC; Du chamber at 24°C at a photoperiod of 16:8 (L:D) Pont). Application rates were 5.0-10.0 ml/liter for and were provided with honey before testing.
Vydate and Lannate and 320-640 I/liter for Asa- Serial dilutions of formulated insecticide were prepared in 50 ml of distilled water plus 1 ml of Long bean (HO and PO) or tomato leaves (PO, 0.2% Triton Ag-98 (Rohm & Haas Company, New- GH) were sampled, brought into the laboratory, ark, N.J.), a wetting agent. Control treatments con- dried at 24°C for 2-3 d, and placed in emergence tained distilled water plus 0.2% Triton Ag-98. Di- cages. Adult parasitoids were aspirated daily from lutions were poured into 36-ml clear plastic cups the cages into glass vials and held at 24°C with and poured back into the original beaker after 10 honey for 1-4 d before the bioassays were done.
s. The cups had an inner surface area of 50 cm2• Because the MO site was a private backyard gar- Treated cups were inverted on a wire rack inside den, plant material infested with Liriomyza was a ventilated hood for 2 h to dry. We estimated that difficult to collect. Therefore, a different technique 95 ± 4.0 mg of solution (n = 10) was deposited on was used to obtain parasitoids for the bioassays.
the inner surface of each cup by weighing the cups Bean plants (12 d old) ('Henderson Bush,' Burpee before and immediately Seed, Warminster, Pa.) grown in a greenhouse in 0.2% solution of Triton Ag-98.
vermiculite and infested with second- and third- Unanesthetized insects set up in untreated cups instar L. trifolii were placed at the MO site for 24 h earlier were gently introduced into the treated 24-48 h. After removal from the field, plants were cups. These cups were then covered with an un- kept in a holding cage in the laboratory for 7-10 treated square of organdy and capped with plastic d. Leaves were removed from the plants, dried, snap-top lid, the center portion removed. A single and placed in emergence cartons. Adult parasitoids drop of honey was placed in the center of the were aspirated and handled in the same manner organdy, and the cup was inverted on a wire screen.
as parasitoids from the HO, PO, and GH sites.
All tests were conducted in an environmental The California D. begini colony was established chamber at 24°C under constant light. Mortality in April 1989 at the Department of Entomology, was recorded at 24 and 48 h. Parasitoids not moving University of California, Davis, from 569 males legs and antennae were scored as dead. On a given and 362 females collected from weeds surrounding date, a series of five or six concentrations plus an a greenhouse in Salinas, Calif. These greenhouses untreated control were tested; each concentration were bordered by artichokes and other vegetable was replicated four times, with five individuals per crops. D. begini were reared at Davis on chrysan- replicate. Experiments were done with ::::120 fe- themum for several generations before overnight males per test date. Tests were rep.eated on at least shipment to Hawaii in June and July 1989. This two different dates (except HO tested with per- ET AL.: INSECTICIDE IN Diglyphus Toxicity of oxamyl and methomylto D. begini Toxicity of fenvalernte and permethrin begini females 5,700 (4,000-16,OOO)d 3,100 (2,700-3,7oo)c 6,900 (5,000-11,OOO)d 1,400 (1,000-1,9OO)b 2,400 (2,000-2,9OO)c • PO, Poamoho, Oahu; HO, Hawaii Kai, Oahu; GH, Glenwood, • PO, Poamoho, Oahu; HO, Hawaii Kai, Oahu; GH, Glenwood, Hawaii; MO, Manoa, Oahu; CA, California.
Hawaii; MO, Manoa, Oahu; CA, California.
b Mg (AI) per liter. LC50'S followed by the same letter are not b Mg (AI) per liter. LC50'S followed by the same letter are not significantly different based on overlap of 95% CL.
significantly different based on overlap of 95% CL.
C LC50 of a population by LC50 of most susceptible by LC50 of most susceptible population (CA).
population (CA).
susceptible population. LC5()and resistance ratio methrin), with data pooled across dates for the data were rounded to two significant digits.
analysis. The MO population was not tested withpermethrin because of the limited number of para- Host Plant Effects. To determine if host plants influenced insecticide susceptibility, D. begini were tions. The CA and MO populations had signifi- reared for one generation in the laboratory on chry- cantly lower LC50's than the three sprayed popu- santhemum and bean before conducting the bioas- lations (PO, HO, and GH) for methomyl, oxamyl, says. Bean leaves from PO infested with Liriomyza and fen valerate. The CA population was the most were collected and dried as described previously.
susceptible to all four insecticides (Tables 1 and 2).
Parasitoids emerging from these leaves were re- The maximum LC50 for oxamyl (HO, 570 mg leased into a Plexiglas-topped wooden cage (122 [AI] per liter) was 20 times higher than the LCso em long, 61 cm wide, and 43 cm high) containing for CA and 8 times higher than the LCso for MO.
12-d-old beans ('Henderson Bush') grown in ver- The maximum Le.o for methomyl (GH, 180 mg miculite or 25-30 cm tall chrysanthemums [AI] per liter) was 21 times higher than the LC.o ida Marble' and 'Iceberg') grown in a 50:50 mixture for the CA strain and 12 times higher than the LCso of potting soil and vermiculite. These plants, in- for MO. The maximum LC.o for fenvalerate (GH, fested with late second- or early third-instar 6,900 mg [AI] per liter) was 17 times greater than trifolii, were exposed to D. begini for 24 h. The the LC50 for the CA strain and five times higher plants were then removed and kept in holding cages than the LC.o for MO. The second highest LCsofor for 7 d to allow the parasitoids to develop. The fenvalerate (PO, 5,700 mg [AI] per liter) was 14 mined leaves were then pinched and placed in times greater than the LC5()for the CA strain. The drying boxes (:::::::17 by 16 by 8 cm) on wire racks maximum LC50for permethrin (GH, 2,400 mg [AI] for 3-4 d before they were transferred per liter) was 13 times higher than the CA strain.
gence cartons. Parasitoids 1-4 d old were used in with Field Rates. All five popu- the bioassays. Individuals were exposed to fenval- lations of D. begini had LCw's below the field rates erate using methods identical to those described for both oxamyl (1,200 mg [AI] per liter) and meth- for field-collected D. begini. Because of an extreme omyl (1,080 mg [AI] per liter). For fen valerate, all male-biased sex ratio, only male D. begini were five populations had LC50'sabove the field rate of available for use in the tests for host plant effects.
240 mg (AI) per liter. For permethrin, population (CA) had an LC50below the field rate with the probit option of POLO-PC (240 mg [AI] per liter). LC50'sfor GH were 29 times (LeOra Software 1987). Control mortality was al- higher than the field rate for fenvalerate and 10 ways <3%. LC.o's were compared among popu- times higher than the field rate for permethrin. For lations to determine intraspecific variability. Dif- the MO and CA populations, LC50'sfor fen valerate ferences were considered significant if 95% CL for were 5.7 and 1.7 times higher than the field rate, the LCso's did not overlap. Resistance ratios were calculated for each insecticide by dividing the LC5() Comparisons Among Insecticides. The trend in of each field population by the LC5()of the most toxicity among insecticides was methomyl > ox- amyl > permethrin > fenvalerate (Tables 1 and Toxicity of fenvalerate to D. begini males 2). All populations tested had lower LCso's for from Poamoho, Oabu (PO) reared from Liriomy"o on different host plants methomyl than oxamyl and lower LCso's for per-methrin and fenvalerate. For the susceptible CA the relative toxicities at LCso were 1:2:14:50 for fenvalerate, permethrin, oxamyl, and methomyl, respectively; methomyl had 50 times greater toxicity than fen valerate. For the resistant GH population, the relative toxicities at LCsowere Long bean (field)" 1:3:16:39 for fen valerate, permethrin, oxamyl, and LCso's followed by the same letter are not significantly different based on overlap of 95% CL.
Host Plant Effects. No significant differences in " Original field collection from long bean.
LCso's for fenvalerate were found between field D.
b Llriomyza begini from bean at PO and D. begini from bean C Llrlomyza at PO reared for one generation in the laboratoryon L. trifolii press) were <8 in 12 of 13 cases (median, 3.1; 2- Bush' bean before testing (Table 3).
12 populations tested per pesticide-species bination). An exceptional case was 66-fold resis-tance to methidathion in a field population Encyrtidae) relative to a laboratory strain of the tions. Three heavily treated populations of D. be- same species (Schoonees & Giliomee 1982). How- gini (PO, HO, and GH) were more resistant than ever, LCso's for two populations of this resistant one untreated population (MO) and one population parasitoid were 12 and 18 times below the rec- with an unknown spray history (CA). The Hawaii ommended field rate. In contrast, LCs;s for resis- data support the hypothesis that variation in treat- tant D. begini were 29- and 100fold higher than ment history caused differences in susceptibility.
the field application rates for fen valerate and per- Large differences occurred between populations on methrin, respectively. These data provide one of Oahu separated by <50 km (distance from MO to the few examples of a hymenopterous PO) and by <16 km (distance from MO to HO), surviving field rates of an insecticide in a laboratory which suggests that local variation in selection was Similar effects of treat- Relative Insecticide ment history on geographical patterns of resistance bioassays indicated that methomyl was highly toxic have also been reported for Aphytis to D. begini compared with oxamyl, permethrin, De Bach (Hymenoptera: Aphelinidae), a parasitoid and fenvalerate.
These data are consistent with of citrus scale (Rosenheim & Hoy 1986) and several results from previous field studies (Oatman & Ken- pests (e.g., Tabashnik et al. 1987, 1990).
nedy 1976; Johnson et al. 1980a,b). Oatman & Ken- Exposure of D. begini to methomyl and oxamyl nedy (1976) reported that methomyl induced leaf- has been considerable in Hawaii. Methomyl, a miner outbreaks because of adverse effects on D.
insecticide, is one of the principal begini and ineffectiveness against Liriomyza materials used to control lepidopterous pests such tivae. Johnson et al. (1980a,b) found that all rates as the tomato fruitworm, Helicoverpa zea (Boddie) of methomyl applied to tomatoes resulted in an and the tomato pinworm, Keiferia increase in leafminer densities and reduced pop- (Walsingham). Oxamyl, also a broad spectrum in- ulations of D. begini. High tolerance of D. begini secticide, has been used for aphid, whitefly, and to fen valerate and permethrin is consistent with leafminer control on vegetables in Hawaii for about tolerance to pyrethroids in other hymenopterous 10 yr (Mau 1983; M.W.J., unpublished data).
parasitoids (Plapp & Vinson 1977, Waddill 1978, Fenvalerate and permethrin have been used ex- Mason & Johnson 1988).
tensively on the United States mainland, but their Host Plant Effect. The results suggest that dif- use on vegetables in Hawaii was limited until 1984 ferences in susceptibility among populations were (Mason et al. 1987). Thus, direct selection of D.
probably caused by variation in insecticide treat- begini by pyrethroids in Hawaii has probably oc- ment history and were not related to host plant curred during the past 5 yr. Cross-resistance may have developed from prior use of chlorinated hy- Conclusions. Our data strongly suggest that D.
drocarbon insecticides such as DDT (Farnham begini in the field has developed resistance to at Sawicki 1976, Vijverberg et al. 1982).
least two pyrethroids and significant resistance to The maximum resistance ratios for D. begini (20 two oxime carbamates in Hawaii in response to for oxamyl, 21 for methomyl, 17 for fen valerate, selection with insecticides. It has been hypothesized and 13 for permethrin) are among the highest re- that parasitoids are slow to evolve resistance be- corded for any parasitoid species. Maximum in- cause they starve or emigrate because of lack of secticide resistance ratios for seven Hymenoptera hosts following insecticide treatments parasitoids reviewed by Tabashnik & Johnson (in 1971, Georghiou 1972). In contrast, Liriomyza RATHMAN ET AL.: INSECTICIDE RESISTANCE IN Diglyphus begini (Mason et a1.
natural enemies: variability and selection. In R. T.
1987) and persist at high densities Roush & B. E. Tabashnik [eds.l, Pesticide resistance spp. are indirect in arthropods. Chapman & Hall, London.
Huffaker, C. B. 1971.
The ecology of pesticide inter- ference with insect populations, pp. 92-107. In J. E.
Swift [ed.l, Agricultural chemicals-harmony in D. begini in Hawaii cord for food people environment. University of Cal- lation of the Hawaiian ifornia Division of Agricultural Sciences Publications, Parasitization of LiTiamyza ability to survive field rates of permethrin spp. infesting commercial and lower rates of oxamyl and methomyl, Hawaii. J. Econ. Entomol. 80: 56-61.
of D. begini may Johnson, M. W., E. R. Oatman & J. R. Wyman.
Lirtomyza spp. leaf miners in manage- ical techniques.
Keil, C. B., M. P. Parrella & J. G. Morse.
We thank M. P. Parrella and K. M. Heinz (University of California, Davis) for providing Diglyphus begini from their California culture. We are grateful to J. F. Brunner (Washington State University) and T. F. Watson (Uni- LeOra Software.
POLO-PC. A user's guide to versity of Arizona) for earlier reviews of this paper. Spe- Probit Or LOgit analysis. Berkeley, Calif.
cial thanks go to L. Oride and L. Caprio for technical Mason, G. A. & M. W. Johnson.
1988. Tolerance to assistance. Yoder Brothers of Barberton, Ohio, supplied permethrin and fen valerate in hymenopterous para- the chrysanthemum plants. This work was supported by sitoids associated with LiTiamyza spp. (Diptera: Agro- the USDA under CSRS Special Grant 88-34135-3600 myzidae). J. Econ. Entomol. 81: 123-126.
managed by the Pacific Basin Advisory Group. This is Mason, G. A., M. W. Johnson & B. E. Tabashnik.
Journal Series 3428 of the Hawaii Institute of Tropical Agriculture and Human Resources Journal Series.
Mason, G. A., B. E. Tabashnik & M. W. Johnson.
Effects of biological and operational factors on evolution of insecticide resistance in LiTiomyza Allen, W. W. & C. A. Charhon.
(Diptera: Agromyzidae). J. Econ. Entomol. 82: 368- of Diglyphus begini and its performance releases on chrysanthemums, pp. 75-81. In D. J. Shus- Tomato insecticide guide for com- ter [ed.], Proceedings Institute of Food and Agricul- mercial producers. Hawaii Institute of Tropical Ag- tural Sciences-Industry conference on biological con- riculture and Human Resources Brief 042.
trol of Liriomyza leafminers. Lake Buena Vista, Fla.
An evaluation of the ef- Croft, B. A. 1990.
Pesticide resistance documentation, fectiveness of established and recently introduced pp. 357-381. In B. A. Croft [ed.], Arthropod biological parasites on LiTiomyza on Oahu, Honolulu. M.S. the- control agents and pesticides. Wiley-Interscience, New sis, University of Hawaii, Honolulu.
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Croft, B. A. & K. Strickler.
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and imigrant chalcid flies of the Hawaiian islands lution of pesticide resistance in natural enemies. In (Hymenoptera). Proc. Hawaii. Entomol. Soc. 5: 418- T. Fisher led.], Principles and application of biolog- ical control. Univ. Calif. Press, Berkeley.
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Received fM publication 29 November 1989; accepted 11 May 1990. Records of the introduced

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