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Hymenoptera: Braconidae), a Parasitoid of the Gypsy Moth (Lepidoptera: Lymantriidae)

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Hymenoptera: Braconidae), a Parasitoid of the Gypsy Moth (Lepidoptera: Lymantriidae) ARTHROPOD BIOLOGY Male-Biased Sex Ratios in Glyptapanteles flavicoxis (Hymenoptera: Braconidae), a Parasitoid of the Gypsy Moth (Lepidoptera: Lymantriidae) ROGER W. FUESTER,1 KENNETH S. SWAN, KYLE DUNNING,2 PHILIP B. TAYLOR, 3 AND GUJJANADU RAMASESHIAH USDAÐARS, BeneÞcial Insects Introduction Research, 501 S. Chapel Street, Newark, DE 19713 Ann. Entomol. Soc. Am. 96(4): 553Ð559 (2003) ABSTRACT Male-biased sex ratios in populations of parasitic wasps used in biological control are undesirable, because a low proportion of females can prevent the establishment of introduced species or hinder commercial production of species used for augmentative control. Studies were conducted on potential factors contributing to male-biased sex ratios that have been encountered in laboratory rearings of the braconid endoparasitoid Glyptapanteles flavicoxis (Marsh) using the gypsy moth, Lymantria dispar (L.), as a host. Sex determination in this wasp is arrhenotokous (haplodiploid). In the Þrst experiment, we stored adults at 13 or 16ЊC and allowed them to mate at 20or 25 ЊC and found that sex ratios (expressed as percentage females) did not differ among progeny of parents; many females produced all male progeny, suggesting that they had not been fertilized. In the second experiment, females were exposed to hosts soon (0Ð60 min) after mating or 23Ð25 h later. Sex ratios were higher (less male-biased) in progenies of females provided with the rest period than in those which were not. In a third experiment, females were allowed to mate from one to four times with a given male. Although differences between these groupings were not statistically signiÞcant, the data suggested that more than two matings might depress sex ratios of progeny. An alternative analysis with only two groupings (1Ð2 matings and 3Ð4 matings) suggested that more than two matings might increase male bias of progeny. Therefore, we suggest that matings of this species be monitored in sleeve cages so that paired females can be removed and separated after copulation to diminish the likelihood of excessive matings, then given a rest period before they are offered hosts for parasitization. KEY WORDS biological control, sex ratio, reproduction, postmating rest period, number of cop- ulations, temperature at mating THE GYPSY MOTH, Lymantria dispar (L.), is one of the lishment (Krause et al. 1991). Because of its gregarious most destructive forest and shade tree pests in the development, large numbers of this parasitoid can be eastern United States. Efforts to obtain biological con- reared with relatively few hosts, and the species was trol of this pest have involved the importation, study, considered to have potential for inundative releases and release of parasitoids (Hoy 1976), predators directed at speciÞc gypsy moth populations (Krause et (Smith and Lautenschlager 1978), and pathogens al. 1991). In fact, G. flavicoxis was reared and released (Elkinton and Liebhold 1990). One of the parasitoids as part of a successful urban forest integrated pest imported for trial against the gypsy moth was Glypta- management (IPM) program for gypsy moth in Vir- panteles flavicoxis (Marsh), a gregarious larval endo- ginia, but Bt and releases of C. melanoscelus were also parasite of Lymantria obfuscata (Walker). Laboratory used in the program, so it is difÞcult to say how much studies in quarantine showed that G. flavicoxis readily G. flavicoxis contributed to suppression (Ticehurst attacked the gypsy moth (Fuester et al. 1987), but it and Finley 1988). Unfortunately, sex ratios in labora- was intrinsically inferior to Cotesia melanoscelus tory rearings of G. flavicoxis are usually male-biased (Ratzeburg), an established braconid, when both spe- (Hu et al. 1986a, 1986b; Fuester et al. 1987; R.W.F., cies parasitized the same host simultaneously (Krause unpublished data). Male-biased sex ratios are delete- et al. 1990). Releases of this species were made in the rious in applied biological control efforts using para- Middle Atlantic States, but did not result in its estab- sitic Hymenoptera, because (1) a reduced number of female founders will decrease the likelihood of estab- 1 E-mail: [email protected]. lishment of imported species used in classical biolog- 2 Current address: 23 Forest Creek Drive, Dover, DE 19904. 3 CABI (Retired), current address: 867, ÔShankarabharanaÕ, 19th ical control, or (2) they make the production of fe- Main, Ideal Homes Township, Rajarajeswarinagar, Bangalore 560098, males too expensive for economical use in an Karnataka, India. augmentative approach. 554 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 96, no. 4 A multitude of factors have been identiÞed as con- Some species of parasitic Hymenoptera require a tributing to male-biased sex ratios in the Braconidae: period of inactivity after copulation to facilitate fer- failure of females to mate (Whiting 1945), refusal of tilization, which does not occur until the sperm older virgin females to mate (Fisher 1964), parental reaches the spermathecal duct and enters the recep- age at time of mating (Pandey and Singh 1998, Run- tacle (Finney and Fisher 1964). Thus, if the females grojwanich and Walter 2000), lack of a postmating rest are exposed to hosts too soon after mating, the sex ratio period and excessive matings (Finney et al. 1947), host in their progeny might be male-biased. In an earlier size or stage (Wong et al. 1990, Tillman and Cate 1993, study (Fuester et al. 1987), we set up males and fe- Pandey and Singh 1999, Kraaijeveld et al. 1999, and males of this species in small cages with caterpillars, so numerous others), host species (Duan et al. 1998), that all mated females were presented with hosts with- host species of origin (Kenis 1996), host plant (Jack- out such a rest period. In our second experiment, we son et al. 1996), host infection with pathogens (Orr et wished to see whether providing a postmating rest al. 1994), maternal crowding (Biswas and Singh 1995), period would enhance the sex ratio of G. flavicoxis. superparasitism (Gul and Gulel 1995), sex ratio of Some species of parasitic Hymenoptera require parents (Zaki et al.1994), clutch size (Vet et al. 1994), only one mating and others require more than one local mate competition (Nishimura and Jahn 1996), (Flanders 1946). In previously published studies by microhabitat (Stark 1991), storage of parents at low Hu (1986a, 1986b) females were left in mating cages temperatures (Jalali et al. 1990), and production of with males for 24 or 48 h. Fuester et al. (1987) placed diploid males (Stouthamer et al.1992). males and females directly in oviposition cages on the With respect to G. flavicoxis, some information is day they emerged from their cocoons. In both cases, available. In laboratory studies using L. dispar as the it was not known how many times females had been host, Hu et al. (1986a) found that the sex ratio, ex- mated. Therefore, our third experiment explored the pressed as a percentage of female progeny, declined effects of multiple mating on sex ratios of G. flavicoxis. with parental female age, but that the adult parental sex ratio (male:female ratio placed in mating cage, not Materials and Methods observed sex ratio among emergees in parental gen- eration), density of females in mating cages, and du- Colonies were started from shipments of G. flavi- ration of time spent in mating cages (24 or 48 h) did coxis cocoons reared from L. obfuscata collected in the not inßuence sex ratios (Hu et al. 1986b). Fuester et Himachal Pradesh province of India during May to al. (1987) conducted laboratory studies on the repro- June, 1999 through 2000, and maintained in the New- ductive response of G. flavicoxis to different instars ark quarantine facility on laboratory-reared gypsy and densities of L. dispar and found that host density moth larvae. Unless otherwise noted, colonies were did not have any effect on sex ratios (percentage of kept in a walk-in environmental chamber at 25 Ϯ 2ЊC females), but that sex ratios in progeny of females and 50Ð60% RH with a 16:8 (L:D) photoperiod. Un- provided with fourth- and Þfth-instar hosts were treated paper-cup containers, 11.5 cm in diameter and somewhat higher than those offered second- and 6 to 7 cm deep (473-ml capacity) with tight Þtting third-instars. Although these studies provided useful clear plastic lids were used for oviposition by parasi- information on factors inßuencing sex ratios, sex ratios toids and for rearing of parasitized hosts. Oviposition reported were still male-biased with mean percent- units contained a 1-oz cup of wheat germ diet for ages of females ranging from 10to 45% (Hu et al. caterpillars, as well as a dental wick moistened with 1986a), 28Ð47% (Hu et al. 1986), and 27Ð40% (Fuester distilled water and droplets of honey on the lid for the et al. 1987). Even the sex ratios with the highest per- parasitoids. Following the oviposition period, adults of centages of females (40Ð47%), were not as high as G. flavicoxis were removed from the units and the those observed in emergence from Þeld-collected gypsy moth larvae left inside until parasite progeny hosts in India (K.W.S., unpublished data). In this pa- emerged, the larva died, or pupation occurred. Rear- per, we evaluate the inßuence of storage temperatures ing units were checked three times a week for removal for adults, temperature in mating chambers, postmat- of frass, depletion of food, and formation of parasite ing rest period, and multiple matings on the sex ratio cocoons. Emerged adults were counted and removed of G. flavicoxis. twice a day (8:00 a.m. and 4:00 p.m.), and adults were Most adult parasitic Hymenoptera can be kept in provided honey and water within 16 h of emergence holding cages in darkness for several weeks at 13Ð16ЊC. and stored at 16ЊC when not being used for experi- Many species of parasitic Hymenoptera mate at tem- mentation.
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