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- Encarsia tricolor Forster (Hym.: Aphelinidae) is an lection; sex ratio dynamics. autoparasitoid of a number of whitefly 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 whiteflies and scale were obtained. (1) A significant positive linear correla- insects, 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, .Encarsia formosa, 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 Brussels sprout 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 Hymenoptera,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