BIOLOGICAL CONTROL 5. 209-217 (1995)

TREVOR WILLIAMSl NERC Institute of Virology and Enuironmental Microbiology, Mansfield Road, Oxford OXl aSR, United Kingdom

Received January 31, 1994; accepted August 18, 1994

autoparasitoid; reproduction; development; host se- tricolor Forster (Hym.: ) is an lection; sex ratio dynamics. autoparasitoid of a number of pest species. Females develop as primary endoparasitoids, whereas males develop hyperparasitica11y in other whitefly en- INTRODUCTION doparasitoids including conspeciflc females. Under a constant regime of25°C and 16:8 h L:D, the biology of E. Aphelinid parasitoid wasps have been among the tricolor was investigated using the Cabbage whitefly, most effective agents in programs of biological control. Aleyrodes proletella, as host. The fo11owing results Against homopteranpests such as and scale were obtained. (1) A significant positive linear correla- , this family of parasitoids has achievedan un- tion was detected between size and longevity for both paralIeled consistency of control in diverse agrosys- sexes, given a honey diet. Mean (:t:SE) longevity was temBoPerhaps the best known example of this is the 16.9 :t 0.62 days for females' and 13.8 :t: 0.66 days for thelyotokous aphelinid, ., and the males. Females were significantly larger than males. whitefly, Trialeurodes vaporariorum, which has be- (2) Female E. tricolor could develop in a11host instars. come a textbook successof biocontrol in glasshouses. Development times were slowest in flrst instar nymphs Of the 860 established releasesfor classical biocontrol (22.3 :t: 0.34 days) and fastest in fourth instar nymphs using parasitoids listed by Greathead(1986), the high- (18.7 :t: 0.25 days). Female development times were not est number, 185,involved aphelinids, of which half suc- overtly variable. (3) Male E. tricolor could hyperpara- ceededin maintaining their target"nostbelow economic sitize a11stages of conspecific female larvae and pupae threshold densities. offered. When parasitizing larvae, male development The reproductivebiology ofmany aphelinid speciesis times were longer, indicating that male development is delayed until the host approaches pupation. (4) Mean remarkable. As welI as showing conventional,bisexual (:tSE) lifetime fecundity of E. tricolor laying female endo/ectophagousdevelopment, aphelinids have been eggs was 85.36 :t: 13.85 at a meRO rate of 7.31 :t 0.27 divided into three groups according to their host rela- eggs/female/day. (5) In a study of sex ratio dynamics tions (Walter, 1983). Females always develop as pri- in the parasitoid culture, emergent sex ratios were a mary endoparasitoidsof Homoptera. Males, however, function of the period of parasitismo The emergent sex developin one of three ways: (i) as primary ectoparasi- ratio (percentage male) from individual leaves in- toids of Homoptera (diphagous parasitoids), (ii) as a creased from 44% alter 2 weeks in the culture to 76o/() hyperparasitoid of an homopteranendoparasitoid (het- alter 4 weeks. A concurrent increase in the overa11per- eronomoushyperparasitoids), or (iii) as a primary en- centage parasitism was al so recorded: 23 ::!:3.4o/() at 2 doparasitoid oflepidopterous eggs(heterotrophic para- weeks to 87 :t 4.1o/()at 4 weeks. (6) Observations on sitoids). oviposition behavior indicated a clear preference to Heteronomoushyperparasitoids have been further exploit late instar nymphs for female production. All divided into varieties of autoparasitoids according to whitefly instars were used for host feeding. Oviposi- the details of male development,but the general term, tion times for male eggs (in conspecific pupae) were autoparasitoid, is often used,as it is here. Such deviant significantly greater than for female eggs (in late in- host relations have marked implications for the use of star whitefly nymphs). «:) 19911Academic Preso, Inc. these parasitoids in control programs, not least be- KEY WORDS: Encarsia tricolor; Aleyrodes proletella; cause,in heteronomoushyperparasitoids, for example, males can develophyperparasiticalIy in conspecificfe- males. Consequently,male production has a negative 1 Current address: El Col~gío de la Frontera Sur, Apdo. Postal 36, impact on the rate of growth of the parasitoid popula- 30700 Tapachula,Chiapas, Mexico. tion.

209 1049-9644/95 $6.00 Copyright @ 1995 by Academíc Press, Inc. AlI rights of reproduction in any forro reserved. 210 TREVOR WILLIAMS

The autoparasitoid, Encarsia tricolor Forster, has mate females. Parasitoids were cultured in conditions been reported from 10 whitefly speciesacross Europe identical to whitefiy, using Brussels plants infested and Russia, most commonlyAleyrodes proletella (But- with A. proletella, added to the culture cage as neces- ler, 1936; Gomez-Menor,1943), Aleurotrachelus jeli- sary. All studies were carried out at 25 :t l°G (16:8 h nekii (Laudonia and Viggiani, 1984), and T. vaporari- L:D), using A. proletella nymphs on orum (Albajes et al., 1980; Arzone, 1976, 1977). As leaves unless otherwise stated. usual, females develop as primary endoparasitoids, whereasmales have beenrecorded as hyperparasitoids Longevity of seven endoparasitoid speciesincluding conspecific Parasitoid pupae were taken from the culture and females (Vet and van Lenteren, 1981; Viggiani, 1984, allowed to emerge in muslin-lidded butter tubs con- 1987;Williams, 1989,1991; Avilla et al., 1991).Because taining dampenedcellulose sponge.Each 24 h, wasps oftheir minute size (ca. 1 mm) and the divergent ontog- were collected, sexed, and transferred to glass vials eny of autoparasitoid species,fundamental studies on containing honey. Vials were examined daily for mor- the biology and reproduction of E. tricolor are few. An tality and fresh honey was added as required. Upon early study by Stüben (1949)described the larval devel- death, the parasitoid head capsulewas measuredat its opment, mating, oviposition, and host feeding behav- widest point to an accuracyof 0.01 mm. This was used iors. Stüben was, however, unaware of sex-linked dif- as an index of parasitoid size. ferencesin developmentand the ability, as with most parasitic ,ofvirgin femalesto lay haploid Female Development male offspring. Later studies have focusedon the po- tential ofthe speciesas a biocontrol agent, particularly Female pupae were placed individually into gelatin in temperature regimes in which E. formosa is not ef- capsules and upon emergencewere allowed to mate fective, or against T. vaporariorum on field crops in with a young male at room temperature. Femaleswere southern Europe (Arzone, 1976; Isart, 1977; Castre- then confined with an abundanceof whitefly nymphs sana Estrada et al., 1979;Bordas et al., 1981; Christo- of a particular instar beneath a clip cage. Clip cages chowitz et al., 1981;Vet and van Lenteren, 1981).Re- were constructed of half a plastic petri dish 35 mm in cent studies of E. tricolor have focused primarily on diameter, 5 mm deep, sealed to the leaf by foam larval developmentin T. vaporariorum and conspecific draught excluder around the edgeof the dish and held or other male hosts (Avilla and Copland, 1987;Artigues in place against the leaf using an elastic bandoMter et al., 1992a,b)or host selection and sex ratio (Avilla 24 h, the parasitoid was removed and the parasitized et al., 1991; Williams, 1991). This work has focused ingscales femaleswere allowed was recorded to develop.daily. The .. pumber of emerg- on the relevante of an understanding of the biology (longevity, fecundity, rates of development, sex ratio dynamics,etc.) of the parasitoid for application to pest Male Developmentin ConspecificHosts control. Leaves bearing third instar whitefly nymphs were exposedto 10 mated females from the culture for 24 h MATERIALS AND METHODS to give a high ratio ofparasitized to unparasitized hosts of uniform age. The female parasitoid larvae so pro- Cabbagewhiteflies, A. proletella, were collectedfrom duced were allowed to develop until early larvae (2-3 Brussels sprout plants (var. winter harvest) during days old), mature larvae (6-7 days old), or young pupae January 1986at Imperial College,Silwood Park, Ascot, (10-11 days old). Each leafwas then offered to a virgin Berkshire, UK. Whiteflies were cultured at 25 :t 1°C female less than 24 h old. Each virgin female could lay (16:8 h L:D) in muslin-walled cagescontaining Brus- male eggshyperparasitically in the parasitized hosts, seIssprout plants 20-30 cm tall, bearing approximately but could only utilize the unparasitized hosts for host- 10 leaves.Parasitoids were collectedby placing plants feeding. AII replicates were allowed to develop until heavily infested with all stagesof A. proletella beneath the primary (female) parasitoids were 12-13 days old, local Viburnum bushes infested with the Viburnum whereupon they were transferred individually to gela- whitefly, A. jelinekii, which is parasitized at low levels tin capsules,checked daily for emergence,and sexed. by E. tricolor (Southwoodand Reader, 1988).After 14 Parasitized scales which failed to emerge were dis- days, the plants were returned to the rearing rooms sectedto determine the fate of their contents. and examined daily for parasitized scales.Additional males were obtained by allowing newly emergedE. tri- color femalesto oviposit in E. formaBapupae on tomato Fecundity leaves from a local glasshouse. Male E. tricolor Single mated femaleE. tricolor were offered an abun- emergedapprQximately 14 days later and were used to dance of third instar whitefly nymphs and transferred BIOLOGY OF E. tricolor IN RELATION TO BIOCONTROL 211 to fresh leaf patches at 48-h intervals until death. To RESULTS ensure successfulmating, a young male was alBopres- ent in the clip cagefor the first 48 h of the experiment, Longevity but not thereafter. Parasitized scaleswere allowed to The mean (:tSE) longevity ofmales was 13.8(:t0.66) develop and emerge as above. Pupae which failed to days (n = 58) comparedto 16.9(:t0.62) days (n = 96) for emerge were included in the fecundity data. Only fe- females.The mean (:tSE) head width was significantly male eggswere laid during the tríal. larger in females (0.243 :t 0.003 mm) compared to males (0.207 :t 0.003 mm) (t = 9.11, df = 152, P < SexRatio Dynamics in the Culture 0.001).This sizedifference was alBoevident in the over- all body size. There was a significant positive linear Leavesbearing all stagesofwhitefly and parasitoids relationship between longevity and body size for both were removedfrom the culture cageon a routine basis: male (t = 2.80,df = 56,P < 0.01)and female (t = 3.89, two leaves per plant per week, with an additional df = 94, P < 0.001)wasps (Fig. 1). Daily mortality data whitefly infested plant being addedto the culture cage were used to construct survival curves for each sex every 2 weeks.The number and sexof E. trícolor adults (Fig. 2). emerging from eachleafwere monitored daily thereaf- ter. Each plant was labeled such that its period of expo- ~emale Development BUfeto parasitism could be recorded. Apart from the All host instars were successfullyparasitized for fe- routine leaf samples,plant material was not removed maleproduction by E. tricolor. On average,in the 24- from the culture cage, except when completely dead h period of exposure,female E. tricolor laid approxi- and devoid of viable parasitoid pupae. As a result of mately five eggs, which is within a range typical for leaf sampling, most plants were defoliated by 4 weeks aphelinids (Viggiani, 1984).Female developmenttime exposure. The culture sampling began with three was negatively correlated with the age of the host, be- plants each separatedby a 1-weekinterval (exposedto ing fastest in fourth instar nymphs (Table 1). These parasitism for 1, 2, or 3 weeks) and the addition of a values are in claseagreement with those of Avilla and single whitefly infested plant marked the commence- Copland (1987) except that they observed fastest fe- ment of the formal sampling. The period of monitoring male development in third instar T. vaporariorum lasted 30 weeks. nymphs at 24°C. The range of developmenttimes for female E. tricolor was not overtly variable within or Oviposition Behavior between replicates, as has been,,1'eportedfor another autoparasitoid species(Flanders, 1939; Broudryk and Young mated females (24-48 h old) with no oviposi- Doutt, 1966; Gerling and Bar, 1971; Donaldsonet al., tional experiencewere placed in pairs on a leaf area 1986). containing an abundanceof all host stages.Each pair was observedfor the following hour and ovipositional Male Development times were recordedusing a stopwatch to an accuracy Becauseof the uniform age of primary hosts offered, of 1 s. When laying female eggs(unparasitized hosts), it was not possibleto detect any preferencefor a partic- all whitefly stageswere offeredsimultaneously in vary- ular host instar for male development.AII stagesof the ing proportions. A plan was drawn of the clip cage conspecificfemale parasitoids offeredwere successfully arena which allowed those nymphs which had been hyperparasitized by E. tricolor. Male developmentwas probed and rejected to be distinguished from nymphs consistently faster than female development, given parasitized successfully.The sequenceand frequency equivalent host stages.As with females, parasitism of ofhost discoveryby eachwasp was alBonoted. Parasit- early host stages causedthe male immature develop- ism was determined by dissection of probed hosts 3-5 ment time to be greatly extended(Table 2). days after the observationswere made.The experiment was replicated 12 times. When laying male eggsin parasitized hosts, female Fecundity E. tricolor were offered leaf areas containing only con- The mean (::tSE) lifetime fecundity of E. tricolor fe- specificpupae and prepupae.AlI pupae which received males laying female eggswas 85.4 (::t13.85)at a mean ovipositional probing during the observation period rate of7.3 (::t0.27)eggs per female per dar. Total mean were transferred individually to gelatin capsulesand eggproduction peakedon Days 3 and 4 of the trial and were dissected3-5 d~yslater for the presenceofhyper- remained high until Day 10, after which it declined. parasitic male larvae. The experiment was replicated These values are in broad agreement with previous five times. studies at lower temperatures. 212 TREVOR WILLIAMS

Females:y=O.93x-S.77 40

35

30

-(lO ;~ 25

'O '-' ~ 20 .~ c= 15 .2 10

5

o

Males: y=O.79x-2.57 40

35

30 . ,-., \1) ;..- 25 ~ . ~ 8 ~ 82 82 . - 20 8 8 '> 8 8 .2 L-- ~ . .2 c 15 . . o . ---. ;.2..~-=-:-~_. 8. .. . 8 10 --:2 . . 8 . . . 8 I . . . 8 . . . 5 8 .

o . I I I I I , , I I I , -'- ' -~. ' ~. 16 1H 20 22 24 26 28 30 32 heud width (mm xl 0-2) FIG. 1. Regressionof parasitoid size as measuredby head width against longevity when maintained individually in tubes on a honey diet without hosts. Figures denoteoverlapping points. Samplesizes, 58 males, 96 females.

Culture Sex Ratio Dynamics Most plante were defoliatedby 4 weeksofleaf sampling which accounts for the reduced sample at Week 5. Sampling leaves at 2, 3, and 4 weeks following their When the samplesfrom each week were pooled, clear introduction to the culture cage yielded a progressively patterns of emergencefor each sex were evident. After more male biased sex ratio (Fig. 3). This was concur- 2 weeksof exposure,leaf samplesdisplayed clear peaks rent with an increasing percentage primary parasitism of emergencefor both sexes,females followed by males. (means ::t:SE): 23 ::t:3.4% at 2 weeks, 63 ::t:6.1% at 3 In subsequentsamples, the peak of female emergence weeks, 87 ::t:4.1% at 4 weeks, and 95 ::t:1.5% at 5 weeks. showeda continual decline whereas the peak of male BIOLOGY OF E. tricolor IN RELATION TO BIOCONTROL 213

liams, 1991)revealed that the frequency of egg encap- sulation in primary or secondaryhosts was consistently very low (1-2%). When offered a choiceof whitefly in- ~ o.e stars, there was a marked preferenceof ovipositing fe- males to exploit late instar nymphs for oviposition (Ta- .> 1.0'~l .~ ~ 0.6" ble 3). AII instars were used almost equally for host (/) " c feeding. o "e Mal~ 8- 0.4" e DISCUSSION a. :\ 'Q. 0.2- ~ A detailed study ofthe biology of E. tricolor confirmed '\ the autoparasitic nature of development.As in other parasitic Hymenopterawith haplo-diploid sex determi- --- -, ~~...:-C~ o 5 in . - 1'5 20 25 35 nation, virgin females can lay haploid male eggs and Age of Wasps (days) can control the sex of their offspring after mating. FIG. 2. Survival curves for each sex of E. tricolor when roain- There was a positive linear relationship betweensize tained on a honey diet without hosts (data froro Fig. 1). and longevity for both sexes.Comparable longevity val- ues in a similar system have been reported for E. cib- ciensis(male, 9.3 days; female, 17.4 days),E. adrianae emergencebecame leptokurtotic; male emergencewas (male, 17.1 days; female, 23.5 days), and E. deserti extended in time. There was no evidence to suggest (male, 18.3 days; female, 22.6 days) parasitizing Be- that the emergencedata were biased by the fact that misia tabaci (Lopez-Avila, 1988). van Lenteren et al. newly emergent females had an opportunity to hyper- (1987) investigated the effect of such diets and host parasitize conspecificsin the interval (up to 24 h) be- plants (cucumber,tomato, and tobacco)on the longev- tween daily collections. If such activity had occurred, ity and fecundity of E. formosa. They found no correla- a distinct secondary peak of male emergenceshould tion, between parasitoid size and longevity in this spe- have been observed Borne14 days after peak female cies. emergence:it was noto Both female and male eggs were able to develop in all stagesof primary and secondaryhosts respectively, Oviposition Behavior although a strong preference t9- exploit late instar whitefly nymphs for female prodúction was detectedin There were clear differences in the times required line with other studies (Artigues et al., 1992b).Develop- to parasitize primary and secondaryhosts. The mean ment times were extendedwhen males or femaleswere (:tSE) drilling and oviposition time for third instar laid in early host stages.When a female eggwas depos- nymphs (210 :t 43.1 s, n = 16) was not significantly ited in a first, second,or third instar nymph, Avilla different from the time required to parasitize fourth and Copland (1987)reported that hatching occurredin instar nymphs (277 :t 78.3 s, n = 24) (t = 0.75, df = the following instar. There are three advantagesto a 38, NS). The mean oviposition time required for laying female parasitoid choosingto oviposit in larger hosts. male eggs in conspecificpupae, however, was signifi- First, she can assessthe host resource exactly with cantly greater than that for fourth instar nymphs (669 regard to size, quality, and suitability at the moment :t 84.1 s, n = 14) (t = 3.41, df = 36, P < 0.001). The of oviposition. Second,eggs laid in early instar hosts dissection results from this and other studies (Wil- will Buffer the same age-relatedmortality risks as the

TABLE 1 Instar Acceptability and DevelopmentTimes for Female E. Tricolor in A. proletella Nymphs

Rangeof Whitefly Mean number oí eggB First pupae seen Mean development development instar Replicates developed/rep(j;SE) (daYB poBtovipoBition) time :t SE (daye) times (days)

1 10 4.9:t 0.69 12 22.3 :t 0.34 18-28 2 10 5.6:t 0.56 11 19.6 :t 0.20 17-24 3 10 6.6:t 1.08 10 19.1 :t 0.24 16-24 4 13 5.5 :t 0.68 9 18.7 :t 0.25 14-24 214 TREVOR WILLIAMS

TABLE 2 Instar Acceptability and DevelopmentTimes for Male E. tricolor Laid in ConspecificFemale Hosts

Age of female host

2-3 days 6-7 days 10-11 days

Number of successfulreplicates 6 5 6 Number of males emerging 41 27 36 Mean developmenttime .i: SE (days) 19.87 :t 0.22 16.48 :t 0.26 14.28:!: 0.14 Rangeof developmenttimes (days) 18-22 15-20 12-16 host (e.g.,predation, disease,etc.). Third, shorter devel- oid pupal casemeant that laying male eggstook about opment times in late instar hosts reducethe period for three times longer than laying female eggs.This repre- which the offspring is susceptibleto hyperparasitism. sents a greater investment in male over female off- The increase in development time of male E. tricolor spring and would be expectedto cause a shift in the laid in young female hosts suggeststhat the male larva sex ratio in favor of females (Fisher, 1930). However, waits until the female larva has grown sufficiently be- such differencesare probably ofminor importancecom- fore hyperparasitic development proceeds. This has pared to the time necessaryto search for, locate, and alBobeen observedin Encarsia perniciosi (Chumakova assesseach type of host. Consequently,inequalities in and Goryunova, 1963)and many indirect autoparasit- oviposition times for eachsex are unlikely to be signifi- oids which lay male eggs in unparasitized primary cant factors in selecting for biased sex ratios in E. tri- hosts in anticipation of future primary parasitism color. In this respect, egg limitation and the relative (Cendana, 1937; Flanders, 1900, 1959, 1969; Walter, availability of male and female hosts are likely to be 1983). Avilla and Copland (1987), however, failed to far more influential (Godfray and Waage, 1991). detect any significant differencesin male development The sex ratio in the culture cagewas strongly influ- times in different conspecifichost stages. encedby the period of exposureof any particular planto There are no data on the frequency of superparasit- The sexratio of E. tricolor emergingfrom leavesshifted ism in this study, although the frequencyofegg encap- from female-biasedafter 2 weeks exposureto a strong sulation was very low both host types. E. tricolor fe- male bias subsequently.This again re!}ectsthe unusual males avoid primary superparasitism except under reproductive strategy of these aphelínids and the inti- conditions of low host availability (Artigues et al., mate relationship between sex ratio and the availabil- 1992b).The proportion and speciesof secondarybosta ity of male and female hosts. It alBodraws attention to available appear to influence the frequency of primary the importance of maintaining abundant material for superparasitism.Primary superparasitismwas overtly female production within cultures ofthese parasitoids. reduced when E. formosa rather than conspecificsec- Failure to do so will rapidly drive the sex ratio to a ondary bosta were offered for male production (Ar- strong male bias resulting in a decreasedyield of para- tigues et al., 1992a).This is algo reflected in a marked sitoid material from the culture (especially females) preference to oviposit in nonconspecifichosts rather and possibly an eventual failure of the culture com- than conspecificsas has been demonstrated in E. tri- pletely. color (Avilla et al., 1991;Williams, 1991)and which is Recently, two autoparasitoid species have been discussedlater. shown to Buffersex ratio disorders such as reported for Female E. tricolor showedratea of egg production in agreement with other studies (e.g., Artigues et al., 1987, 1992a).Like many aphelinid species(Jervis and TABLE 3 Kidd, 1986), adult E. tricolor are synovigenic and Ovipositional PreferencesWhen a Choiceof Whitefly emerge with very few mature oocytes,typically 0.8- Instars Was Offered to InexperiencedE. tricolor Females 2.6. Femalesmust host-feedbefore full eggmaturation can occur. No relationship betweenthe number ofma- Whitefiy instar ture oocytesat emergenceand parasitoid size or subse- First Second Third Fourth quent fecundity has been found in E. tricolor (Avilla and Copland, 1988),although a strongly positive corre- Total number encountered 95 35 80 latían has been reported for fecundity in E. formosa Number parasitized O O 16 24 (van Lenteren et al., 1987). Number drilled but rejected O 1 23 33 5 7 The extra effort required to drill through the parasit- Number used for host feeding 3 5 BIOLOGY OF E. tricolor IN RELATION TO BIOCONTROL 215

AFTER 2 WEEKS OF PARASITISM 300 Oyera\! Sex Ratio=0.44 250 Oyeral. Percentage Parasitism=23% 200 (n=30 leayes) CI) ~ Q. 150 ~ < ~ CI) u. 100 ~ 50 o UJ -J O 15 20 25 30 35 40 8 Q. ~ o a: u. >- ~ a: UJ Q. " Z ¡; a: UJ ~ UJ

~ , AFTER 4 WEEKS OF PARASITISM (5 1- 150j Overall Sex Ratlo=O.76 ~ < a: Overall Percentage Parasitism-S7% < Q. (n~24 laRvas) u. o a: ~ 30 35 40 45 50 ~ ;:) AFTER 5 WEEKSOF PARASITISM Z ] Overall Sex Ratlo=0.61 -J SO < ~~~ O:erall percentage Parasltlsm=95% 1- O 40 45 50 55 (n=6 leaves) g

DA YS SINCE INITIAL EXPOSURE TO CUL TU RE

FIG. 3. Daily emergence of male (bars) and female (lines) E. tricolor from leaves exposed to parasitism in the culture cage for 2-5 weeks. Data on parasitoids emerging from leaf samples were pooled at each time point to give total sample sizes of 3677 parasitoids after 2 weeks of parasitism, 4132 after 3 weeks, 1965 after 4 weeks, and 398 after 5 weeks. several other parasitoids, most notably the pteromalid dence of sex ratio disorders in this species (M. S. Nasonia vitripennis (e.g.,Skinner, 1982;Werren et al., Hunter, personal communication). 1986;Nur et al., 1988).Affected E. pergandiella diploid Of additional relevanceto the biocontrol ofwhiteflies (female) eggs will deve10pas semifunctional haploid is that E. tricolor has been reported to show a marked males following loss of the paternal genomefrom the preferenceto exploit non-conspecificsover conspecifics egg. Consequently,in this species,males can deve10p for the production of males. This was not apparently and emergefrom primary as well as secondaryhosts due to size or developmentaleffects of males emerging (Hunter et al., 1993). In the norma11ythe1yotokous E. from another species, but may be a mechanism by formaBa,large numbers of males have been produced which female E. tricolor avoid hyperparasitizing their following antibiotic treatment suggestinga cytop1asmi- own progeny (Avilla et al., 1991; Williams, 1991). cally inherited microorganism as the causative agent Clearly, the possibility that autoparasitoids may have (Zchori-Feinet al., 1992).How commonsuch afflictions a highly negative impact on conventional speciesal- are among heterononious aphe1inidsis unknown, a1- ready parasitizing a particular whitefly pest should be though examination of E. tricolor has revealed no evi- considered.The result of such hyperparasitic attack on 216 TREVOR WILLIAMS alternative endoparasitoid populations should be orum Westwood(Homoptera, Aleyrodidae). Anales del Inst. Nac. carefully assessedbefore introduction of the autopara- Inuest.Agrar., Serie:Protec. Veg. 11, 57-65. Cendana,S. M. 1937.Studies on the biology of Coccophagus(Hym.) sitoid; host-parasitoid-autoparasitoid population mod- a genus parasitic on nondiaspidine coccidae.Uniu. Calif. Pubs. els could be of great predictive value in this respecto Entomol. 6, 337-399. Christochowitz,E. E., van de Fluit, N., and van Lenteren,J. C. 1981. ACKNOWLEDGMENTS Role of developmentand ovipositionfrequency of Trialeurodesua- porariorum, Encarsia formaBa(2 species)and E. tricolor at low I am indebted to Jeff Waagefor his help and advice during the glasshousetemperatures. Med. Fac. Landbouww.Rijksuniu. Gent courseof this study. I am grateful to the staff of Imperial College, 46,477-485. SilwoodPark, for their assistancewith the supply of plant material Chumakova,B. M., and Goryunova,Z. S. 1963.Development ofmales for this study and for maintenanceofthe culture rooms,etc. Dr. Andy of Prospaltellaperniciosi Tow. (Hym. Aphelinidae),parasite of San Polaszekof IIE identified parasitoids and gave advice on aphelinid JoseScale (Hom. Coccidiae).Entomol. Reu.42, 178-181. . Dr. Jesus Avilla and Dr. asear Alomar both provided Donaldson,J. S., Clark, M. M., and Walter, G. H. 1986. Biology of helpful information at the start of the study. This work was part of the heteronomouehyperparasitoid Coccophagusatratus Compere a NERC Studentship awardedto JeffWaage. (Hymenoptera:Aphelinidae): Adult behaviour and larval develop- mentoJ. Ent. SocoSth. Afr. 49, 349-357. REFEREN CES Fisher, R. A. 1930. "The Genetical Theory of Natural Selection." Oxford Univ. Preee,pp. 158-160. Albajes,R., Casadevall,M., Bordas,E., Gabarra, R., and Alomar, O. Flanders, S. E. 1936. Remarkable phenomenonof reproduction in 1980.La moscablanca de los invernaderos,Trialeurodes vaporari- the parasitic Hymenoptera.J. Econ. Entomol. 29, 468. orum en El Maresme.11. Utilizacion de Encarsia tricolor (Hym., Flandere,S. E. 1939.The propagationand introduction of Coccopha- Aphelinidae) en un invernadero de tomate temprano.Anales del gus heteropneusticusComp., a parasite of lecaniine ecaleineecte. Inst. Nacional Invest. Agras Agricola 13, 191-203. J. Econ. Entomol. 32, 888-890. Artigues, M., Avilla, J., Sarasua,M. J., and Albajes,R. 1987.Encar- Flanders, S. E. 1959.Differential host relations of the sexesin para- sia tricolor v's Encarsia formaBa:Their use in biologicalcontrol of sitic Hymenoptera.Entomol. Exp. Appl. 2, 125-142. Trialeurodesvaporariorum in Spanishconditions. Int. Union Biol. Sci. WPRSBull. lO, 18-22. , Flanders, S. 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