BIOLOGICALANDMICROBIALCONTROL

Effects of Pyriproxyfen on Three Species of Encarsia(Hymenoptera: Aphelinidae), Endoparasitoids ofBemisia argentifolii (Homoptera: Aleyrodidae)

TONG-XIAN LID ANDPHILIP A. STANSLY

Southwest Florida Research and Education Center, University of Florida, P. O. Box 5127,Immokalee, FL 34143-5002

J. Econ. Entomol. 90(2): 404-411 (1997)ABSTRACT Effects of the phenoxy juvenile hormone analog pyriproxyfen were evaluatedin the laboratory on larvae, pupae, and adults of the endoparasitoids Enearsia pergancliellaHoward, E. transvena (Timberlake), and E. formosa Gahan, as well as on their host, Bemisiaargentifolii Bellows & Perring. Although B. argentifolii nymphs reared on sweet potato leavesand treated as 1st, 2nd, or 3rd instars with pyriproxyfen developed to the pupal stage, $500 million in 1992, and >$142million in Florida (Perring et al. 1993). Althoughinsecticides are used widely to control B. argenti-folii, the potential of biological control to reducewhitefly populations through colonization fromsurrounding habitat (Stansly et al. 1994) or inun-dative release (Parrella et al. 1992) has been dem-onstrated. This potential might be integrated intoconventionally managed systems by substitutingbroad-spectrum insecticides with selective materi-als that interfere only minimally with the activitiesof the most effective natural enemies.

Insect growth regulators (IGRs) have been usedextensively in management of Bemisia on cotton inIsrael (Ishaaya and Horowitz 1992, Horowitz andIshaaya 1994). One of these, buprofezin with chitin

synthesis inhibitory activity, has been shown to berelatively innocuous to Eretmocerus sp. and En-carsia luteola Howard, endoparasitoids of B. tabaci(Gerling and Sinai 1994). Pyriproxyfen is a juvenilehormone analog with relatively low mammaliantoxicity (Yokoyama and Miller 1991) that was firstregistered in Japan in 1991 for controlling publichealth pests (Miyamoto et al. 1993). The utility ofpyriproxyfen in whitefly management was demon-strated based on suppression of embryogenesis andadult formation in B. tabaci (Ishaaya and Horowitz1992) and Trialeurodes vaporariorum (Westwood)(Ishaaya et al. 1994). McMullen (1990) found thatpyriproxyfen was safe to predators of pear psylla,Cacopsylla pyricola Foerster, such as Anthocorisantevolens White, A. nemoralis (F.), Deraeocorisverbasci Uhler, Campylomma verbasci (Meyer-Dur), and Chrysopa spp. However, pyriproxyfen at12.5 mg (AI)/liter inhibited growth and develop-ment of Cryptochaetum iceryae Williston, a para-sitoid fly of cottony cushion scale, Icerya pllrchasiMaskell, and caused total suppression of egg hatch

0022-0493197/0404-0411 $02.00/0 © 1997 Entomological Society of America

April 1997 LIU AND STANSLY: EFFECTS OF PYRIPROXYFEN ON Encarsia SPP. 405

of Elatophil!ls. hcbroiclls Pericart, a predator ofMatS!lCOCCIlSjosephi Bodenheimer & Harpaz(Mt'lldel et al. 1994). Some economically impor-hUlt coccinellid biological control agents have alsobeen found to be highly sensitive to pyriproxyfen(Hattingh lUld Tate 1995). Pyriproxyfen was con-sidered "very harmful" to pupae, and "slightlyhannfu]" to adults of E. formosa in the KoppertSide Effect List (Anonymous 1995).

Our objectives were to evaluate insecticidal ac-tivity of pyriproxyfen on B. argentifolii, and com-patibility of this insect growth regulator with someprincipal parasitoids of the whitefly in the genusEncarsia.

Materials and Methods

Bemisia argentifolii Culture. B. argentifolii wasobtained originally from D. J. Schuster (Universityof Florida, Bradenton) in 1990, and was identifiedas B. tabaci biotype 'B' in 1992 and as B. argen-tifalii in 1994. The colony has been maintainedsince tllen in a greenhouse culture on various pot-h'd host plants including the following: collard,Brassica alcrocca L. variety acephala, 'Georgia LS';hibiscus, Hibiscus rosa-sinellSis L., 'Brilliant Red';salvia, Salvia splendcns L.; and sweet potato, Ipom-oea batata (1,.) Lam., 'Carolina Bunch'. Plantswere grown singly in 15-cm pots in Metro-Mix 300grO\ving medium (Grace-Sierra, HorticulturalProducts, Milpitas, CAl and watered weekly with0.1 % (wt: vol) of Stem's Miracle-Gro (N: P: K, 15:30:15) (Stt'm's Miracle-Gro Products, Port Wash-ington, NY).

Encarsia Kpp. Culture. Encarsia pergandiellaHoward (identified by G. A. Evans, University ofFlorida, Gainesville) was initially obtained fromthe whitefly colony that had been parasitized fromnatural sources in 1993, and later maintained in50-cm:l wood frame cages enclosed with 52-meshLumite polyethylene screen (Chicopee, Gaines-ville, GA). Encarsia tronsvena (Timberlake) fromthe surrounding environment displaced E. pergan-diclla in the greenhouse colony in 1995 and wassubsequently maintained in the same type ofwoodt'n cages. Encarsia formosa Gahan was pro-vided by J. Nelson (University of California, Davis)from a greenhouse colony of B. argentifolii onpoinst'ttia (Ertphorbia prtlcherrima Wild.), and alsowas maintained on B. argentifolii in wood framecagt's. Voucher specimens of parasitoids and white-Hies wcre deposited in the insect collection atSOllthwt'st Florida Research and Education Cen-ter, Univt'rsity of Florida at Immokalee.

Individual sweet potato leaf cuttings were usedas hosts for B. argentifolii in all experiments.LeaVl's wt'rt' cut from the vine and the petiole in-serted into root cubes (3.75 cm3, OASIS GrowingMedium, Smithers-Oasis, Kent, OR), then placedin plastic trays (T. O. Plastics, Minneapolis, MN;52 by 26 by 6 cm) into which water and fertilizer(0.1% Miracle-Gro) were added once a week. Ex-

periments were conducted in an air-conditionedinsectary at 26.7 ± 2°C, 55 ± 5% RH, and a pho-toperiod of 14:10 (L: D) h. Light intensity wasmeasured as photosynthetically active radiation at39-44 JLmolm-2 S-1 inside cages (Steady State Po-rometer, Model LI-1600, LI-COR, Lincoln, NE).

Whitefly Cohorts. Sweet potato leaves wereplaced in 0.9-liter clear plastic cups, each with anopening (9 em diameter) opening on top screenedwith nylon organdy and a corked access hole (1.2cm diameter) on the side. Whitefly adults aspiratedfrom the greenhouse colony were introduced foroviposition periods of 24 h (whitefly experiments)or 12 h (parasitoid experiments). Cohorts were in-spected daily until desired stages had been ob-tained-6 d for 1st instar, 9 d for 2nd instar, 11 dfor early 3rd instar (appropriate for parasitization),15 d for 4th instar, and 18 d for pupae (red-eyednymphs).

Effects on B. argentifolii. Pyriproxyfen(S-56716, 0.83 EC; Sumitomo, Osaka, Japan) wasused in all experiments at 3 concentrations of 1.00,0.05, and 0.01 mg (AI)/liter with water (reversedosmosis, 7 ppm solid) as control. The 2 lower con-centrations were chosen on either side of the 0.04-mg (AI)/liter rate reported by Ishaaya and Horo-witz (1992) to cause 91% suppression of adult de-velopment when applied to 2nd and 3rd instars ofB. tabaci. An additional rate of 1.00 mg (AI)/literwas included to test for possible effects of highconcentrations on parasitoids.

Leaves containing appropriate whitefly cohortswere dipped in the 3 pyriproxyfen dilutions or wa-ter control for 5 s and allowed to air dry for 1 h.Leaves were reconfined in the cup cages for in-cubation in the insectary and evaluated for adultemergence after all live whiteflies had emerged.Each treatment for each stage had 10 single-leafreplicates.

Parasitoid Cohorts. Sweet potato leaves infest-ed with 3rd instar whitefly (11 d old) cohorts wereplaced into cup cages. Ten parasitoid females (plus2-3 males in the case of E. pergandiella and E.trallSvena), collected with an aspirator from green-house and insectary colonies, were placed intoeach cup cage for a 24-h oviposition period. Adultwasps were removed, and parasitoid cohorts wereallowed to develop into appropriate stages fortreatments.

Treatment of Parasitoid Larvae. Parasitoidcohorts were incubated for 6 d after removal ofadult wasps and examined under a stereoscopicmicroscope to identify 20 parasitized whiteflynymphs containing 2nd- or 3rd-instar parasitoidlarvae that were circled with an india ink pen oneach of 8 leaves per treatment per parasitoidspecies. Leaves were dipped for 5 s in dilutionsof 1.00, 0.05, and 0.01 mg (AI)/liter pyriproxyfenor a water control, air dried for 2 h, and individ-ually confined in cup cages. Newly emerged par-asito ids were removed to prevent possible mor-tality of remaining pupae through host feeding

406 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 90, no. 2

and oviposition. Parasitoid emergence was eval-uated 2 wk after parasitization, and emergedadults were examined for physical abnormalitieswith the stereoscopic microscope.

Treatment of Parasitoid Pupae. Sweetpotatoleaves containing cohorts of parasitized whiteflieswere monitored daily until parasitoids had pupated(11 d after removal of wasps). The leaf surface inproximity to each parasitized pupa was markedwith india ink for identification, and leaves weredipped in pyriproxyfen, dried, and incubated asabove. Emergence and mortality of the markedparasitoid pupae were evaluated 1 wk later by mi-croscopic examination, and adults were examinedfor physical abnormalities. Each rate of pyripro-xyfen was applied to 8 leaves (replicates) for eachparasitoid species with 29.8 ± 2.5 (mean ± SE;range, 17-4:2) pupae on each leaf.

Developmental Rate of Parasitoid Imma-lures. Treatments were applied 24 h after the endof the 24-h parasitization period when parasitoideggs were 1-2 d old. Leaves bearing parasitizedwhitefly nymphs were immersed in the 3 pyriprox-yfen dilutions or water control for 5 s, air dried,and incubated as above. When the parasitoid lar-vae became visible through the whitefly cuticle(usually 7 d after parasitization), 20 parasitizednymphs were identified on each leaf with india inkdots on the nearby leaf surface. Parasitized nymphswere examined daily with the stereoscopic micro-scope until all parasitoids either died or emerged.There were 4 replicates (leaves), or a total of 80parasitized nymphs for each treatment X parasit-oid combination.

Treatment of Parasitoid Adults. Sufficient E.pergandiella were not available, so only E. formosaand E. transvena were used for this experiment.Parasitoid adults were confined to the abaxial leafsurface in clip cages made from a 12-ml polysty-rene medicine cup on which the bottom (2.5 cmdiameter) had been replaced with a 60-mesh plas-tic screen. A metal hair clip was glued to the cupand held the mouth (4.0 cm diameter) in contactwith the leaf surface. A cohort of whitefly eggs wasestablished by introducing 60 whitefly adults (sexundetermined) from the greenhouse culture into

. each clip cage for a 24-h oviposition period. White-fly adults were removed, and ""150 nymphs wereallowed to develop within each clip cage for 11 d(early 3rd instar). Leaves were dipped in 1 of 3concentrations of pyriproxyfen for 5 s, and airdried for 4 h. Female parasitoids (15-18) (plus 2-3 males of E. transvena) were introduced into eachclip-on cage, and mortality was evaluated 24 h lat-er. Whitefly nymphs were recaged, and parasitiza-tion and emergence of parasitoid adults were re-corded after 2 wk under a stereoscopicmicroscope. Each treatment X parasitoid combi-nation had 8 replicates (leaves).

Second-Generation Effects. Based on resultsfrom the experiments described above, E. formosawas selected as the most susceptible of the 3 spe-

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April 1997 La; AJ\'D STANSLY: EFFECTS OF PYRIPROXYFEN ON Encarsia SPI', 407

Tabl.· 2. P"rt"'ntallie (mean ± SE) emer!'ienee of adult Enearsia SI'I'. from B. argelltifolii treated with I'yril,roxyfen6.5 dafter l18rasitization

Ratl'. E'l'l'rgmulil'lIa E. trlIllsr;cna E.jorl1losamg (AIlI

EIllt.'r~('net' Emergence EnH'r~('ll('('litO,O,~ 167 96.4 :t 1.4a 313 98,8 :t 0,6" 164 94.4 :t 1.8ao,m 241; 98.4 :t 0,8" 212 97.4 :t 1.3" 143 97.9 :t l.la\\'ater 213 97.2 :t l.la 248 98,0 :t l.la 164 99.3 :t 0.7a

\'allll's ill till' sam.' column with the same letter do not differ significantly (f > 0.05 rSAS Institute 1988]).

cies tested, A 6-d-old cohort of E, formosa wastreated with 3 dilutions of pyriproxyfen or the wa-ter control (8 single-leaf replications each) as de-scribed above, Development was monitored daily,and 10-11 newly emerged adult females «48 hold) were aspirated from each treatment into cupcages containing sweet potato leaves infested with"'200 third-instar B. argentifolii each for a 24-hoviposition period. This test had 4 replications,Parasitoid emergence from the succeeding gener-ation was recorded 3 wk later.

Data Analysis. Numbers of parasitized, unpar-asitized-Iive, and unparasitized-dead whiteflynymphs expressed as percentages in all experi-ments were analyzed using the general linear mod-el (PROC GLM), and means were separated usingthe Fisher protected least significant differencetest (LSD) (SAS Institute 1988), Percentage emer-gence fell between 0 and 30% in the experimenton parasitoid pupae; therefore, corresponding pro-portions were transformed to their arcsine V be-foTt,~Ulalysis(Gomez and Gomez 1984),

Results

Effects on B. argentifolii. Affected whiteflynymphs appeared to develop normally, but died inthe pupal stage, turning dark and wet, Responseto pyriproxyfen decreased with whitefly age attreatment-no emergence if treated as 1st and 2ndinstars, 69% emergence if treated as 4th instars, and>98% emergence if treated as pupae-which wasnot significantly different from the water control(Table I), Third- and 4th-instar B. argentifolii ex-hibited significantly increased response to greaterconcentrations of pyriproxyfen,

Effects on Parasitoid Larvae. Emergence of E,pergandiella was unaffected by application of pyr-iproxyfen to nymphs parasitized with 6,5-d-old lar-vae at the tested rates, whereas emergence of E.formosa was reduced by the greatest (1.00 mg [AI]/liter) concentration applied (Table 2), The re-sponse of E. transvena appeared to be intermedi-ate but was not significantly different from thewater-treated control. Affected E, formosa failed toemerge, although those that did emerge appearednormal, Abortive pupae appeared normal at firstbut later desiccated and shrank.

Effects on Parasitoid Pupae. Pyriproxyfen pro-duced no noticeable response in E, pergandiellaand E. transvena when applied to whitefly nymphscontaining pupae of these species, and parasitoidsemerged normally (Table 3). In contrast, pyriprox-yfen applied to the pupal stage at rates of 0,05 and1.00 mg (AI)lliter reduced emergence of E. for-mosa by 44.6% and 73.5%, respectively, althoughresponse to 0,01 mg (AI)/liter was not Significantlydifferent from the water control. Deformed wings,particularly front wings, were observed on "'40%of E, formosa adults emerging from pupae treatedwith 1.00 mg (AI)lliter pyriproxyfen (Fig, I), Asidefrom their inability to fly,deformed wasps behavednormally in regard to grooming, searching, prob-ing, host-feeding, and oviposition.

Developmental Rate of Parasitoid Imma-lures. Significant increases in developmental pe-riod from oviposition to emergence were ob-served in all 3 parasitoid species tested inresponse to applications of pyriproxyfen made towhitefly nymphs 1 d after parasitization (Table4), Developmental time was lengthened in re-sponse to the greatest rate by 10.2% for E. per-gandiella and 20,7% for E. transvena. Increases

Tllbl" 3. Per"entnllie (mean :t SE) emer!'ience of adult Encarsia spp. from B. argentifolii treated with )lyriproxyf,,"U.5 d nftE'r pnrllsitizlltioll (pnrnsitoids in pupul stage)

Rat.' E. I'l'rgalldidla E. trallSvena E·formosamg (AIlI

EIIl!"rgenc!" Emergence Erll('rg:(,lK'('litt'r n II II

l.OO 2i5 97.6 :t 1.2a 277 99.4 :t 0.6" 327 26.5 15.4cO.ll5 176 100.0 :t O,Oa 202 100,0 :t 0.0" 287 55.4 10BbO.()l 239 99.7 :t 0.2a 253 100,0 :t O.Oa 247 94.8 1.I:Ia\V"tt'r 143 98.6 :t O,8a 277 100,0 :t 0.0" 160 100.0 O,Oa

Values in tilt' same column with tlle'same I!"tters do not differ significantly (f > 0,05, LSD [SAS Institute 1988]).

408 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 90, no. 2

Fig. 1. Wings of female E. fomwsa. (A) Normal front wing and hind wing. (B-C) Abnormal front wing amI hindwing (D-F) Abnormal front wing.

in development time of E. pergandiella occurredin the pupal stage, whereas pupal stage, egg, andlarval stages of E. transvena and E. formosa werelengthened. Mortality was low for all treatments,ranging from 0 to 2 individuals within each spe-cies X treatment group, with no obvious trendsamong species or treatments.

Effects on Parasitoid Adults. No statisticallysignificant mortality of adult E. transvena and E.fornwsa was observed in response to contact withresidues of pyriproxyfen. However, these data sug-gested a low-level response, especially by E. hr-rrwsa (Table 5).

Unexposed wasps successfully parasitized morewhitefly nymphs than exposed wasps, significantlyso in the case of E. formosa (F = 3.36; df = 3,28; P = 0.0326), which were more susceptible to

pyriproxyfen than E. transvena (F = 3.48; df = 3,28; P = 0.029). Reduction of progeny per femalewas significantly reduced by 30.7 and 42.3% withE.formosa and by 21.7-29.3% for E. transvena inthe 2 greater rates. Emergence of subsequentprogeny was significantly reduced for both SPt'-cies-27.6% reduction for E. formosa at thegreatest rate, and 11.0% for E. transvena at thesame rate.

Second-Generation Effects. Parasitization ofwhitefly nymphs by E. formosa wasps treated aslarvae with 1 mg (AI)/Iiter pyriproxyfen was sig-nificantly reduced by 58.6%, and a reduction of48.2% was evident with the 0.05 mg (AI)/Iitcr ratt~(Table 6). A 21.4% reduction at the 0.01 mg (AI)/liter rate showed the same trend although the dif-ference was not significant. Emergence of sub-

April 1997 LlU AND STANSLY: EFFECTS OF PYRIPROXYFEN ON Encarsia spp, 409

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410 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 90, no. 2

Table 6. Parasitization of B. argentifolii by E. for-mosa wasps treated as larvae with pyriproxyfen

No. No.Ratt', .. 't white. Progeny % reo % emer-(AI)l p.If,IS'· A'mg.. aid les. per duction gencelit". 'i! paraslt·

Ized

1.00 44 196 4.5 :!: 12.1b 58.6 90.70.05 44 245 5.6 :!: 14.9b 48.2 91.30.01 44 363 8.3 :!: 6.8ab 21.4 93.1'Vater 44 273 10.8 :!: 24.9a 0.0 97.6

Progeny per (mean:!: SE) followed by the same letters donot diff". Si~liRc"ntly (P > 0.05, LSD [SAS Institute 1988]).

sequent progeny was not significantly affected butalso tended to decrease.

DiscussionThere is much that we do not yet understand

about the response of Encarsia species to pyriprox-yfen. Why is uniparental E. formosa more sensitiveto pyriproxyfen than biparental E. pergandiella andE. transvena in terms of adult development andembryogenesis? Why does toxicity increase withage of the E. formosa immatures at time of expo-sure, whereas the opposite is true of its whiteflyhost? The sensitivity of early instars of Bemisia topyriproxyfen is shared by several species of scaleinsect, including California red scale, Aonidiellaaurantii (Maskell); Florida wax scale, Ceroplastesfioridensis Comstock; and cottony-cushion scale,lcenja purchasi Maskell (Peleg 1988, 1989),whereas other species, including mosquitos(Schaefer et al. 1988) and even the greenhousewhitefly, Trialeurodes vaporariorum (Westwood)(Ishaaya et al. 1994), are more sensitive whentreated as late instars.

In contrast to other parameters evaluated, theresponse to pyriproxyfen treatment 36 ± 12 h afteroviposition was greatest for E. transvena, least forE. pergandiella, and intermediate for E. formosa.We anticipated a response for E. pergandiella, be-cause females oviposit in Ist-instar B. argentifoliibut egg eclosion or early larval development (orboth) is delayed or arrested until the host reachesthe 3rd instar (Liu and Stansly 1996). Could de-layed development of E. pergandiella in Ist-instarnymphs be a response to high host titers of juve-nile hormone? Perhaps E. pergandiella cannotmake molting hormone and may depend insteadon molting hormone from the host. If so, the effectmight be mimicked by treatment with pyriproxy-fen. However, we observed an increase develop-ment time of the egg and early larval stage in Ist-instar hosts, whereas only an increase in the pupalstage of E. pergandiella was observed in responseto pyriproxyfen. However, both egg and larvalstages of E. transvena and E. formosa were length-ened by treatment with pyriproxyfen. One factorobscuring the comparison is that treatment oc-

curred as much as 48 h after oviposition, so thatmany parasitoid eggs may have already maturedpast the point of sensitivity to pyriproxyfen at thetime of application. Further research will be re-quired to clarify the relationship between delayeddevelopment of parasitoids in young-instar hostsand in hosts treated with juvenile hormone ana-logue.

Despite mysteries surrounding mechanisms ofpyriproxyfen selectivity, we now have better infor-mation to integrate the use of this material in con-junction with biological control of B. argentifolii bythe 3 Encarsia species tested. No deleterious ef-fects were noted on adult emergence to E. per-gandiella or E. transvena at the rates applied toparasitized whitefly nymphs, although a modestlengthening of development time was observed.Also, contact toxicity to adult E. transvena wasminimal, although some suppression of subsequentparasitization and adult emergence was noted.Therefore, pyriproxyfen could be applied withminimal deleterious effects when these 2 speciesare the principal natural enemies. This is a fortu-nate result, given that crops are currently colo-nized by these species from sources within thehabitat. However, pyriproxyfen should not be ap-plied when E. formosa is in its later stages of de-velopment. Because colonization by E. formosa isusually from commercial sources, parasitoid re-leases and pyriproxyfen applications could be co-ordinated to avoid deleterious effects to late-stageparasitoid immatures. However, a detrimentaleffect on the next generation could be expected.

Pyriproxyfen is known to be extremely persistenton citrus and highly detrimental to some coccinel-lid species and therefore disruptive to biologicalcontrol of mealybugs and cottony cushion scale oncitrus in South Africa, albeit at higher rates (30 mg[AI]/liter) than we used for whitefly control (Hat-tingh and Tate 1995). The Encarsia species wetested represent a single component of the naturalenemy complex surrounding B. argentifolii. Thenet effect of foliar applications of pyriproxyfen onthe entire complex must be evaluated before ageneral compatibility with biological control couldbe affirmed.

Acknowledgments

WethankJ. L. Nationand H. J. McAuslane(Universityof Florida, Institute of Food and AgriculturalSciences)and R. D. Oetting (Universityof Georgia, Griffin) formanuscriptreviews,and J. M. Conner,Y. M. Zhang,andT. Yost for technical assistance.This study was in partfundedby USDACompetitiveGrant No.93-34103--8433and ValentCorporation,WalnutCreek, CA. FloridaAg-riculturalExperimentStationJournal SeriesR-05262.

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Received for publication 8 August 1996; accepted 2 De-cember 1996.

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