Inter- and intra-specific host discrimination in gregarious and solitary endoparasitoid wasps

In nature, most species of Lepidoptera are attacked by parasitoids, and some species may be hosts for several parasitoid species. When hosts are parasitized by more than one female of the same species (=superparasitism) or females of different species (=multiparasitism), then intrinsic competition occurs for control of host resources. To reduce competition, some parasitoids are able to recognize the difference between parasitized and unparasitized hosts. Inter- and intra-specific host discrimination were investigated in the two sympatric species, the gregarious Cotesia kariyai (Watanabe) and solitary Meteorus pulchricornis (Wesmael), endoparasitoids of the Oriental armyworm Mythimna separata (Walker). To measure host discrimination, choice experiments were conducted in which females of both species foraged and chose between healthy host larvae and hosts initially parasitized by either C. kariyai or M. pulchricornis. An olfactory test was also performed to examine the discrimination behavior of the two parasitoids. Our results showed that, in oviposition choice tests, both braconid female wasps were able to discriminate between unparasitized hosts and from four to seven day-old hosts previously attacked by conspecific and heterospecific wasps. On the other hand, superparasitism and multiparasitism occurred even in host larvae that were parasitized two days earlier. However, once the immature parasitoids hosts are at larval stage (1st and 2nd instar), super- and multiparasitism were avoided in the two-choice test, but the latter often occurred in the multiple-choice experiment. Host discrimination abilities may have been based on plant volatile signals incurred from damaged plants and internal mechanisms from four to seven post-parasitized hosts.     

寄主大小及寄生顺序对蝇蛹佣小蜂寄生策略的影响

寄主大小模型认为寄生蜂后代性比与寄主大小相关,寄生蜂倾向于在大寄主上产出更多雌性后代,在小寄主上产出更多雄性后代.探讨了以家蝇蛹为寄主时,蝇蛹佣小蜂后代产量和性比变化;单次寄生情况下,寄主大小及寄生顺序对寄生蜂后代性比等影响.结果表明,蝇蛹佣小蜂的产卵期为(8.93±3.34)d,单头雌蜂能产雌性后代(34.11±16.34)头和雄性后代(11.04±8.87)头,且雄性百分比为0.24±0.11.随成蜂日龄的增大,寄生蜂产生雄性后代的比率显著增加.蝇蛹佣小蜂在寄生家蝇蛹时,会优先选择寄生个体较大的蛹;在单次寄生的情况下,蝇蛹佣小蜂倾向于在较大的家蝇蛹内产出更多的雌性后代.     

螟蛉盘绒茧蜂的过寄生行为及其对子代生长发育的影响

【目的】过寄生现象普遍存在于寄生蜂寄生过程中。本研究旨在探究螟蛉盘绒茧蜂Cotesia ruficrus的过寄生对子代发育的影响及影响过寄生行为的主要因素。【方法】室内研究了螟蛉盘绒茧蜂在其寄主稻纵卷叶螟Cnaphalocrocis medinalis3龄幼虫上过寄生行为的发生,不同产卵次数对寄主存活及子代蜂生长发育的影响,研究了不同接蜂时间和不同接蜂密度对过寄生发生的影响。【结果】螟蛉盘绒茧蜂存在过寄生行为,无论雌蜂有无产卵寄生经历,均能在被自身寄生过和同种不同个体寄生过的寄主内产卵。寄生蜂茧量随着被产卵次数的增加而增加,被产卵3~5次的寄主体内死亡的寄生蜂幼虫数随着增大。寄主在育出蜂前的死亡率随着被产卵寄生次数的增加而增加,被产卵5次时,寄主育出蜂前死亡率达50%。过寄生使螟蛉盘绒茧蜂子代蜂卵-蛹的历期延长,羽化率和雌雄性比下降,雌蜂体型随寄生次数的增加显著变小。过寄生率随着接蜂密度及接蜂时间的增加而增加。【结论】在寄主上产卵2次对螟蛉盘绒茧蜂子代发育是最适合的,产卵3次及以上为过寄生。过寄生使蜂子代发育适合度降低,不利于子代生长发育。在室内大量繁殖螟蛉盘绒茧蜂时,应减少接蜂密度和接蜂时间,从而减少过寄生的发生。     

Oviposition decisions in an endoparasitoid under self-superparasitism conditions

Superparasitism is a widespread phenomenon. Having accepted superparasitism, mated female parasitoids must decide on the sex of each egg they subsequently lay into the same host. Theory predicts that this decision is either based on host quality, when more male eggs are laid in hosts that are already parasitized because they are perceived to be of poorer quality; or more eggs are laid of the sex that is most likely to be a strong larval competitor, i.e. generally females.Anastatus disparis is a facultative endoparasitic egg parasitoid. We used ‘artificial’ hosts to explore outcomes of decision making by A. disparis during superparasitism under a manipulated absence of larval competition. When only one egg was laid it was always female. As the number of eggs laid increased, so more of them were male. This supports the theory that oviposition decisions are based on host quality; more male eggs were laid in hosts that were already parasitized and thus of poorer quality.In a second experiment, eggs were exposed to parasitoids for different periods of time. Half the eggs were dissected to determine the number of parasitoid eggs that had been laid. The remaining eggs were incubated and the number and sex of offspring that ultimately emerged, following larval competition, were recorded. Under superparasitism conditions fierce larval competition ensued; only one offspring survived and they were predominantly female.In conclusion, oviposition decisions by female A. disparis accepting self-superparasitism were made based on host quality.     

Superparasitism limitation in an aphid parasitoid: cornicle secretion avoidance and host discrimination ability

Superparasitism avoidance by the endoparasitoid Aphidius rhopalosiphi De Stefani Perez on the grain aphid, Sitobion avenae was studied. Experiments were carried out in which aphids were exposed to two consecutive attacks by parasitoids. Results showed that superparasitism avoidance in A. rhopalosiphi was mediated by two successive stimuli whose effectiveness depended on the time interval between attacks. For short time intervals (<16 h), host rejections were mainly associated with the presence of dried cornicle secretion on the host's body which was exuded during the first attack. The repellency of this secretion declined with the time interval between attacks, becoming ineffective 2 days after the first parasitization, and allowed females to reject up to 30% of parasitized hosts. For longer time intervals (>/=16 h), host rejection behavior was a response of parasitoid females to internal changes in host quality associated with parasite development. This response gradually increased with an increase in time interval, reaching no more than 60%, 96 h after initial parasitization. This host discrimination ability did not allow females to distinguish between hosts parasitized by themselves or by conspecifics. Consequently, these findings suggest that superparasitism is a common event in A. rhopalosiphi and especially on recently parasitized hosts.     

State dependent superparasitism in a solitary parasitoid: egg load and survival

In solitary parasitoids, superparasitism (the allocation ofan egg to an already parasitized host) has a payoff, measuredin offspring produced and costs, measured in eggs and time invested.Solitary parasitoids that are capable of host discriminationmust adopt the strategy that ensures the best use of both theiregg load and available lifetime. In this paper, we develop astate-dependent model defining the optimal strategy of superparasitismfor a solitary parasitoid species with overlapping generations.The fitness measure we use is based on the growth rate of thenumber of genotype copies. The model predicts that the tendencyto superparasitize should increase as the egg load of the parasitoidincreases, or as its life expectancy decreases. The model alsopredicts that under particular conditions wasps should showpartial preferences for parasitized hosts. These predictionswere tested with the parasitoid Venturia canescens (Hymenoptera:Ichneumonidae). The tendency of the wasps to superparasitizein the presence of both healthy and parasitized hosts was correlatedto egg load and access to food before the experiment A complementaryexperiment, where parasitized hosts were given sequentiallyto parasitoids, showed that V. canescens exhibits partial preferencestoward superparasitism. These experimental results and a previouswork support the predictions of the model.     

Food-deprived host-feeding parasitoids kill more pest insects

Some parasitoids not only parasitize their hosts but also destructively feed on them which could result in host mortality. We hypothesized that host-feeding parasitoids that are food-deprived before being released for biological control would destructively feed on more hosts, and an optimal duration of food deprivation of parasitoids would enhance host feeding without negatively affecting parasitism. We investigated the effects of food-deprivation durations (0, 3, 6, 10, 24 h and 20% honey solution offered), before being released, on the host mortality and parasitism by a destructive host-feeding parasitoid of whitefly nymphs, Encarsia sophia (Girault & Dodd) (Hymenoptera: Aphelinidae). In another experiment, we compared host feeding, parasitization and longevity throughout the lifespan between food-deprived and non-food-deprived parasitoids. Using fourth-instar Bemisia tabaci B biotype as the host, the responses of E. sophia differed significantly with the durations of food deprivation before they were exposed to their hosts. E. sophia adults food-deprived for 6 h killed more hosts through feeding than those that were food-deprived for 0, 3, 10 and 24 h or those that were fed with honey solution. Moreover, parasitoids that were food-deprived for 6 h parasitized more hosts than those held for other durations of food deprivation. Similar results on host-feeding were found when third-instar whitefly nymphs were used. We confirmed that E. sophia food-deprived for 6 h not only killed more whiteflies through host feeding, but also lived significantly longer and parasitized more hosts than the non-food-deprived ones throughout their lifespan. Our results could be extended to improve the effectiveness of augmentative biological control of pests through improved host feeding and parasitizing capacity by starving the parasitoids for a certain period of time before they will be used.     

Adaptive superparasitism in solitary parasitoids: marking of parasitized hosts in relation to the pay-off from superparasitism

Abstract.

• 1 The pay-off from an egg laid in a parasitized host is an important parameter in models on adaptive superparasitism in solitary insect parasitoids.
• 2 For Leptopilina heterotoma, a parasitoid of larval Drosophila, the pay-off from a second egg laid in a host is 0.43 offspring when the interval between the two ovipositions is less than 3h. For longer intervals, this pay-off decreases to almost zero for an interval of 24 h.
• 3 When a female encountering a parasitized host is able to estimate the interval since the first oviposition, it is expected that she will take this into account in her host selection decisions. This is, however, not in the direct interest of the female that lays the first egg, and marks the host.
• 4 We studied whether superparasitism in hosts containing a young egg is more common than in hosts containing an older egg, when searching in a patch containing once-parasitized and unparasitized hosts.
• 5 The acceptance/encounter ratio of parasitized hosts increased for intervals longer than 6h, as predicted when the interests of the marking female and the longevity of the mark are taken into account.
• 6 Superparasitism occurred more often when parasitoids had previously searched a host patch 7 days before the experiment compared to when parasitoids had searched a patch 1 day before, a phenomenon predicted by dynamic optimal diet models.

     

Sex Allocation Decision Under Superparasitism by the Parasitoid Wasp Eupelmus vuilleti

Superparasitism is a widespread phenomenon in parasitoids and may be advantageous in some circumstances. In this study, offspring sex ratio was analysed in three superparasitism situations: when the second egg was laid by a random Eupelmus vuilleti (Hymenoptera: Eupelmidae) female from a group, when an isolated female was allowed to lay two eggs on the same host (self-superparasitism) or laid one egg on a host already parasitized by a conspecific (conspecific superparasitism). Females produced a different offspring sex ratio according to the different superparasitism situations tested. These sex ratios are in line with the local mate competition theory. The results further suggest that females can discriminate between hosts parasitized by a conspecific or by themselves and adapt the sex of the eggs they lay accordingly.     

Interspecific interference competition between Encarsia formosa and Encarsia sophia (Hymenoptera: Aphelinidae) in parasitizing Bemisia tabaci (Hemiptera: Aleyrodidae) on five tomato varieties

Abstract Interspecific competition between Encarsia formosa and Encarsia sophia, two major parasitoids of Bemisia tabaci, and the influence of five tomato varieties on competition outcome were investigated under laboratory conditions. E. formosa parasitized more B. tabaci than E. sophia when in single wasp assays on any of the tomato varieties investigated. When B. tabaci nymphs were exposed to both wasp species (either simultaneously or sequentially), the number of B. tabaci nymphs parasitized by either wasp species was significantly decreased compared to the sole access condition. Total mortality of B. tabaci was increased when B. tabaci nymphs were exposed to both wasp species compared to only one wasp species. Thus competition between E. formosa and E. sophia apparently reduced parasitoid offspring numbers, but not the efficiency of biological control. In fact, control efficiency was enhanced in some cases, particularly on tomato variety Huangtuoyuan (HTY). When wasps were allowed sequential access to hosts, interference occurred through host feeding by the second wasp, especially if it was E. sophia. The effect of different tomato varieties was not significant.     

Parasitism byEphedrus cerasicola [Hym.: Aphidiidae] developing in different stages ofMyzus persicae [Hom.: Aphididae]

The parasitoidEphedrus cerasicola Stary oviposited in the 4 nymphal instars and in newly moulted apterous adults ofMyzus persicae (Sulzer). Development and reproduction of unparasitized and parasitized aphids at 21°C were compared. Unparasitized aphids developed to adults in 6.5 days and started to reproduce after 7 days. Longevity varied between 7 and 42 days. Net reproductive rate (R₀) was 40.7. In contrast to older nymphs, aphids parasitized in the 1 st instar almost never reached the adult stage before mummification. Aphids parasitized in 2nd, 3rd and 4th instar and as newly moulted adults produced respectively 0.07 %, 2 %, 23 % and 32 % of offspring produced by unparasitized aphids. Corresponding reproductive periods were 1, 1.4, 3 and 4 days. Host age at parasitization had a slight effect on the parasitoid's developmental rate and had no effect on egg or pupal survival, or on the sex ratio of the emerging parasitoids.     

Superparasitism and host size effects in Oomyzus sokolowskii, a parasitoid of diamondback moth

Many aspects of a parasitoid's biology may be affected by its host. Host size, for example, could affect parasitoid fitness, especially in gregarious parasitoids, in which the resource is used by multiple siblings. Oomyzus sokolowskii (Kurdjumov) (Hymenoptera: Eulophidae) is a gregarious larval–pupal endoparasitoid of the diamondback moth, Plutella xylostella L. (Lepidoptera: Plutellidae), a major pest of crucifers worldwide, and is able to superparasitize the host. This study focuses on the hypothesis that because resource availability is higher in larger hosts, parasitoids developing in larger hosts will fare better. However, superparasitized hosts are expected to yield larger numbers of parasitoid offspring of smaller body size. Results showed that superparasitism increased the number of parasitoid offspring produced per host and increased offspring longevity, but decreased offspring body size. However, developmental time and sex ratio of parasitoid offspring was similar among hosts parasitized once, twice, or three times. Regardless of superparasitism, parasitoids emerging from larger hosts that were fed honey solution lived longer than similarly fed progeny from smaller hosts (36.4 vs. 22.1 days). The results partially support the hypothesis that Oomyzus gained fitness from an increase in host size; moreover, superparasitism seems advantageous for Oomyzus due to increased offspring numbers and longevity.     

Effect of the primary host for production of both sexes on the mating interaction in an autoparasitoid species

Encarsia sophia (Girault and Dodd) is an autoparasitoid in the hymenopteran family Aphelinidae. The females develop as primary parasitoids on whitefly nymphs (primary hosts), whereas the males develop as hyperparasitoids on their own species or on other primary parasitoid species (secondary hosts). The autoparasitoids not only parasitise whiteflies but also kill them with strong host-feeding capacity. In this study, female and male E. sophia were reared on the primary hosts Trialeurodes vaporariorum and Bemisia tabaci ‘Q’, and the host-feeding and parasitism of wasps on both whitefly species were determined for the four possible different mating combinations: (i) E. sophia females reared on B. tabaci (ESF-BT) mated with E. sophia males from B. tabaci (ESM-BT), (ii) E. sophia females reared on T. vaporariorum (ESF-TV) mated with E. sophia males from T. vaporariorum (ESM-TV), (iii) ESF-BT mated with ESM-TV, and (iv) ESF-TV mated with ESM-BT. ESF-TV mated with ESM-TV killed the largest percentage of whitefly nymphs through host feeding. The ESF-TV with larger body size mating with larger ESM-TV killed more whitefly nymphs through host feeding than those mating with smaller ESM-BT. Whether B. tabaci or T. vaporariorum were used as hosts, ESF-TV mated with ESM-TV and ESM-BT and ESF-BT mated with ESM-BT significantly parasitised more whitefly nymphs than ESF-BT mated with ESM-TV. In general, ESF-BT mated with ESM-TV killed significantly fewer whitefly nymphs through parasitism and host feeding than the other three mating combinations on both whitefly species. These results indicated that the performance of autoparasitoids on insect pests was not only dependent on females but was also affected by mating with males from different primary host species.     

Adaptive self- and conspecific superparasitism in the solitary parasitoid Leptopilina heterotoma (Hymenoptera: Eucoilidae)

One of the foraging decisions facing parasitoids is whetherto accept (superparasitize) or reject hosts that have alreadybeen parasitized. An important distinction is whether the hosthas been parasitized by the female parasitoid herself or bya conspecific. In solitary parasitoids, the pay-off from anegg laid in the latter host type (conspecific superparasitism)is the probability that the second egg wins the competitionfor the host and results in an offspring. The pay-off from anegg laid in the former type (self-superparasitism) increaseswith an increasing probability that another female will superparasitizethe host in the near future. When this probability equals one,self-superparasitism and conspecific superparasitism have thesame payoff. However, conspecific superparasitism will generallyhave a higher pay-off than self-superparasitism. It will thereforebe beneficial for a female parasitoid to be able to distinguishbetween a host she parasitized and one parasitized by a conspecific.The degree of benefit depends on the probability of conspecificsuperparasitism in the near future. Using an optimal diet model,I show that when a parasitoid encounters a patch containinga mixture of unparasitized and already-parasitized hosts, afemale that can distinguish between the two types of parasitizedhosts gains more offspring than a female without this ability.However, when parasitoids search a patch together with conspecifics,it is adaptive to self-superparasitize, and the pay-off fromthis ability may be negligible. It is therefore predicted thatwhen a female parasitoid searches a partially depleted patchalone, it will reject the hosts parasitized by itself more frequentlythan hosts parasitized by conspecifics. In contrast, femaleparasitoids searching together are predicted to accept hoststhat they parasitized themselves much more often. The resultsshow that the solitary parasitoid Leptopilina heterotoma (Hymenoptera:Eucoilidae) is able to distinguish between hosts that it parasitizedand hosts parasitized by conspecifics. The predictions of themodel are met in a second experiment that shows that L. heterotomaself-superparasitizes when the probability of conspecific superparasitismis high.     

Sex allocation and effects of superparasitism on secondary sex ratios in the gregarious parasitoid, Trichogramma chilonis (Hymenoptera: Trichogrammatidae)

The role of sex-controlling behaviour at oviposition in generating primary sex ratios, and the effect of larval competition on secondary sex ratios, were studied in the gregarious endoparasitoid, Trichogramma chilonis. The production of a fertilized (female) egg is indicated by the incorporation of a pause in abdominal movements during oviposition, while the absence of it indicates the production of an unfertilized (male) egg. During each ovipositional bout, the first male egg is deposited at the second oviposition, and thereafter at intervals of about eight eggs. This simple pattern enables the wasps to adjust their progeny sex ratios under local male competition to a wide range of host size. Inexperienced wasps do not distinguish between parasitized and healthy hosts. Immature mortality is not significantly different between the sexes when a host is attacked by a single wasp, while females suffer higher immature mortality than males when superparasitism occurs.     

Host discrimination modulates brood guarding behaviour and the adaptive superparasitism in the parasitoid wasp Trissolcus semistriatus (Hymenoptera: Scelionidae)

Because hosts utilized by parasitoids are vulnerable to further oviposition by conspecifics, host guarding benefits female wasps. The present study aims to test whether female adults regulate brood guarding behaviour by host discrimination in a solitary parasitoid Trissolcus semistriatus by presenting an intact or parasitized host egg mass to a female adult. Virgin females without oviposition experience have host discrimination ability, which enables them to adjust the number of eggs laid in the hosts. Mating experience increases superparasitism by female adults, whereas mated females achieve a higher discrimination ability as a result of oviposition experience and show a lower superparasitism rate. As expected, females exhibit brood guard after parasitizing an intact host egg mass, whereas those females visiting a previously parasitized host egg mass, do not. Because the survival of eggs in superparasitized hosts is relatively low, regulating brood guarding behaviour by host discrimination is adaptive for female wasps.     

Sublethal effects of chlorantraniliprole and thiamethoxam seed treatments when Lysiphlebus testaceipes feed on sunflower extrafloral nectar

The extrafloral nectar (EFN) of sunflower, Helianthus annuus L., is an important summer resource for many insects and represents a potential route of exposure to systemic insecticides applied as seed treatments to cultivated varieties. Among the many parasitoids that utilize sunflower EFN, Lysiphlebus testaceipes (Cresson) (Hymenoptera: Braconidae) is an important generalist parasitoid of cereal aphids in North America. This study evaluated the performance of adult wasps fed EFN of sunflower plants grown from seed treated with chlorantraniliprole and thiamethoxam. Consumption of EFN from treated sunflower seedings caused no lethal effects, but reduced the numbers of greenbug nymphs, Schizaphis graminum Rondani, attacked and parasitized when wasps foraged in Petri dish arenas. Whereas control females self-superparasitized every fourth host, those exposed to chlorantraniliprole did not. Offspring developmental time and adult emergence were unaffected by either treatment, but thiamethoxam greatly reduced the proportion of female offspring.     

Effects of the mixed biocide Bacillus thuringiensis–abamectin on the development of the parasitoid Microplitis mediator and its host Helicoverpa armigera

The effects of the mixed biocide Bacillus thuringiensis Berliner with abamectin (BtA) on the development of the parasitoid Microplitis mediator (Haliday) (Hymenoptera: Braconidae) and its cotton bollworm host, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), were evaluated in the laboratory. Weight gain in larvae of H. armigera was initially delayed, but larval developmental period increased and pupal weight increased when they were fed on a diet containing BtA. Due to increased longevity of the host larvae, the susceptible period to parasitization of H. armigera by M. mediator increased when the host larvae were reared on diets containing BtA at concentrations of 0.5, 1, 2, and 4 μg g^?1. The longevity of female and male parasitoids significantly decreased when newly emerged wasps were fed a honey solution containing 200 μg ml^?1 BtA in comparison with those fed only a honey solution. Mean longevity was significantly prolonged when parasitoids were fed a honey solution and BtA–honey solution in comparison with those fed BtA–distilled water, distilled water, or nothing. There were no significant differences compared with the control in any biological characteristics for the offspring of female parasitoids fed the honey solutions containing BtA at concentrations of 50, 100, and 200 μg ml^?1; characteristics measured include the egg‐larval period, pupal weight, male and female pupal periods, adult fresh weight, and adult longevity. When female parasitoids parasitized host larvae that had been fed the diet containing BtA, their male and female pupal periods were significantly prolonged compared with the control (without BtA).     

A large-scale rearing method for Peristenus digoneutis (Hymenoptera: Braconidae), a biological control agent of Lygus lineolaris (Hemiptera: Miridae)

Releases of Peristenus digoneutis against Lygus spp. in North America have been conducted for many years; however, no published procedures for mass production of the biological control agent were available. A laboratory rearing method was developed using Lygus lineolaris as the host to enhance establishment efforts and provide large numbers of wasps for inundative releases into high value fruit crops. Experiments were conducted to determine optimum host:parasitoid density and rearing temperature. The effects of nymph:wasp ratios and temperature on parasitism and wasp survival showed a 20:1 ratio at 20°C provided high parasitism (256 parasitized nymphs/wasp over lifetime) and excellent wasp survival of 27 days. Experiments on diapause-inducing conditions for P. digoneutis demonstrated that fluctuating temperatures of 23°C (day) and <16°C (night) and corresponding photo phases of 16 h light, for rearing parasitized nymphs, produced 100% diapausing parasitoids whereas non-diapausing parasitoids were only produced at more than 16 h light. Furthermore, parasitized Lygus nymphs need to be transferred to short day conditions no later than 10 days after parasitism to produce diapausing parasitoids. Critical life stages for exposure to conditions inducing diapause, the egg, first and second instar parasitoid larva, occurred from 0 to 10 days at 24°C constant temperature. Increased time in cold storage reduced the number of days to first emergence of parasitoids from diapausing cocoons when transferred to warm temperatures. The optimum storage time for diapausing P. digoneutis is between 25 and 44 weeks, depending upon the length of time that cocoons remain at warm conditions prior to chilling.     

Fitness consequences of ovicide in a parasitoid wasp

Ovicide, superparasitism and host rejection are alternative reproductive tactics facing female parasitoid wasps encountering an already-parasitized host. Superparasitism is simply the addition of an egg or a clutch of eggs by the secondary parasitoid, but under ovicide the primary clutch is removed or destroyed. Host rejection occurs if the wasp leaves without laying a clutch. The ectoparasitoid Laelius pedatus (Say) (Hymenoptera: Bethylidae) performs ovicide in this situation. Clutch manipulation experiments show that secondary clutches suffer high mortality in competition with primary clutches, which increases with increasing time delay between clutches. Primary clutches however suffer little in competition with secondary clutches, even if there is minimal time delay between clutches. These data suggest that the offspring of ovicidal females are substantially fitter than the offspring of superparasitizing females. Handling time and clutch size do not differ significantly between first (sole) parasitoids and second (ovicidal) parasitoids. The same is true for offspring survival and development time. However, offspring of second females are slightly smaller. This suggests that parasitized and unparasitized hosts are resources of similar quality when ovicide is performed. These data strongly support the predictions of evolutionary models of ovicide. They may also give some insight into the taxonomic distribution of ovicide in parasitoids.