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.

     

Superparasitism as a differential game

Superparasitism refers to a female parasitoid laying an egg in a host already parasitized by a conspecific. In solitary species, only one offspring per host is expected to complete development, hence the game. Hosts are often clumped in patches and several females exploiting such an aggregate of resource make its state change over time, hence the dynamical character of the game. Two coupled questions arise: (i) Is it worth accepting a parasitized host? (ii) When to leave the host patch? Through these decisions (i) the competition for healthy hosts and (ii) the trade-off between leaving in quest of a better patch and staying to make the patch less profitable for other parasitoids (this is a way to lower superparasitism likely to occur after having left the patch) are addressed. The aim of this work is to characterize a strategy that would be evolutionarily relevant in such a situation, as it directly concerns females' reproductive success. Investigating a (synchronous) nonzero-sum two-player differential game allows us to characterize candidate dynamic evolutionarily stable policies in terms of both oviposition and patch-leaving decisions. For that matter, the game is (in the most part of the parameter space) completely solved if the probability that superparasitism succeeds is assumed to be close to one-half, a fair value under direct competition. The strategic equilibrium consists, for each females, in (i) superparasitizing consistently upon arrival on the patch, and (ii) leaving when the loss of fitness due to superparasitism likely to occur after its departure is reduced to zero. The competing females are thus expected to leave the patch as they arrived: synchronously. Superparasitism does not necessarily lead to a war of attrition.     

Adaptive significance of facultative infanticide in the semi-solitary parasitoid Echthrodelphax fairchildii

Abstract.  1. This is the first work to show how imperfect kin recognition influences the behavioural strategy of parasitoids.
2. The female of Echthrodelphax fairchildii lays an egg on the right or left side of the host thorax. When superparasitising on the side without the first offspring, it often probed the opposite side with its sting and killed the first offspring more than 50% of the time. The frequency of probing increased with increasing inter-oviposition interval, and was higher in conspecific superparasitism than in self superparasitism.
3. The adaptiveness of probing was assessed by the difference in fitness returns between superparasitism with probing and superparasitism without probing. Fitness returns from self‐superparasitism and those from conspecific superparasitism were assessed by the fitness performance of both first and second comers, and that of second comers respectively.
4. In terms of the survival rate of immatures (one fitness component), probing under conspecific superparasitism guaranteed higher fitness returns than not probing for longer oviposition intervals, but under self‐superparasitism not probing guaranteed higher fitness returns for shorter intervals because superparasitism for such intervals often resulted in two-adult emergence.
5. In terms of head width (another fitness component), probing produced higher fitness returns for shorter oviposition intervals for both self and conspecific superparasitism.
6. Assuming that offspring quantity contributes more to fitness returns than does offspring quality, the observed frequencies of probing were considered adaptive for parasitoids whose abilities to distinguish between self and conspecifically parasitised hosts and to estimate inter-oviposition intervals are imperfect.     

Superparasitism strategy in a semisolitary parasitoid with imperfect self/non-self recognition, Echthrodelphax fairchildii

To assess the adaptiveness of self‐ and conspecific superparasitism in the parasitoid Echthrodelphax fairchildii Perkins (Hymenoptera: Dryinidae), we measured the rate of superparasitism avoidance and fitness returns from superparasitism for different intervals between the first and second ovipositions. We also tested for any preference in oviposition side and whether any such preference was adaptive. The rate of superparasitism avoidance in both self‐ and conspecific superparasitism was about 10% for oviposition intervals of 2–8 h, and higher for intervals of 1 and ≥24 h (but did not exceed 35%). When conspecifically superparasitizing (but not self‐superparasitizing), females exhibited a slight preference for the side without the first‐comer. Under conspecific superparasitism, the survival rate of second comers was independent of the oviposition side and interval, but slightly lower than that of immature parasitoids for single parasitism. The adult size of second‐comers on the side harboring the first‐comer was larger than that of second‐comers on the side without it, when the oviposition interval was <24 or 96 h. These results explained the overall low rate of avoidance of conspecific superparasitism, but not the variation in avoidance rate or the preference for side without the first‐comer when conspecifically superparasitizing. Assuming that fitness returns are influenced more by offspring quantity than by their quality, self‐superparasitism produced positive fitness returns only when the oviposition interval was <24 h and the side without the first‐comer was selected. This suggests that the observed behavior was not adaptive. Possible reasons for the discrepancies between observed and optimal behaviors, including an imperfect ability for self/non‐self recognition, are discussed.     

Presence of a conspecific increases superparasitism but not infanticide under self‐ and conspecific superparasitism in a semisolitary parasitoid,Echthrodelphax fairchildii (Hymenoptera: Dryinidae)

Female parasitoids are expected to avoid superparasitism (ovipositing in and/or on parasitized hosts) when unparasitized hosts are available. However, when the supply of unparasitized hosts is restricted, they are expected to self‐ as well as conspecifically superparasitize. One of the cues of a reduced availability of unparasitized hosts is the presence of a conspecific. Moreover, if the focal species can perform infanticide, after encountering a conspecific female, the females are expected to kill eggs existing in and/or on hosts when superparasitizing, because the eggs are more likely to be laid by others. In this study we investigated whether females of an infanticidal semisolitary parasitoid, Echthrodelphax fairchildii, increase their frequencies of superparasitism and infanticide after encountering a conspecific female. Echthrodelphax fairchildii females are capable of discriminating between self‐ and conspecific superparasitism until up to 0.75 h after the first egg was laid (self‐superparasitism frequency < conspecific superparasitism frequency). As expected, the female parasitoids were more likely to perform self‐ and conspecific superparasitism after they had encountered a conspecific. In particular, the self‐superparasitism frequency increased highly within a short period after the first oviposition, so that no difference between the self‐ and conspecific superparasitism frequencies was found. In contrast, the infanticidal‐probing frequency remained extremely low, irrespective of whether or not the female parasitoids had encountered a conspecific. Moreover, when superparasitizing, females usually laid female eggs. Possible causes for the low frequency of infanticidal probing and the female‐biased sex ratio are discussed.     

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.     

Artifical transfer and morphological description of virus particles associated with superparasitism behaviour in a parasitoid wasp

In parasitoids, the adaptive significance of superparasitism (laying of egg(s) in already parasitized hosts) has been the subject of strong controversy. The current view is to interpret this behaviour as an adaptation to increased competition for hosts, because the supernumerary egg still has a chance to win possession for the host. However, we recently discovered that in the solitary parasitoid Leptopilina boulardi, superparasitism is rather caused by an unknown infectious element: stable non superparasitizing lineages (NS) are transformed into stable superparasitizing lineages (S) after eggs from both lineages have competed inside the same host (superparasitism). In this report, we investigate the nature and location of the causative agent. Involvement of bacteria is unlikely because antibiotic treatments do not affect wasp phenotype and because bacterial 16S ribosomal DNA was not detected using PCR. We report successful injection experiments showing that the causative agents are located in wasp poison gland and ovaries and are stably inherited. Electron microscopic studies demonstrate that long filamentous virus particles located in wasp oviducts are strongly associated with superparasitism behaviour, leading to reconsider the adaptive significance of this behaviour in parasitoids. Interestingly, parasitoids are often infected with similar viruses for which no phenotypic effect has been documented. This raises the possibility that they could induce the same behavioural manipulation.     

Asymmetric larval competition between two species of solitary parasitoid wasps: the influence of superparasitism

Abstract.

• 1 We test the hypothesis that a solitary parasitoid wasp may gain in fitness if she lays more eggs in a host.
• 2 Using heterospecific superparasitism (=multiparasitism) between the solitary aphid parasitoids, Aphidius smithi Sharma & Subba Rao and Ephedrus californicus Baker, we show that (i) a superparasitizing female's chance that her offspring will survive competition is an increasing function of egg density, and (ii) survival among same-aged larvae is independent of the oviposition sequence.
• 3 These findings on asymmetric larval competition provide indirect evidence that supports two fundamental, but untested, assumptions underlying models of adaptive superparasitism between conspecific wasps.

     

Self-/conspecific discrimination and superparasitism strategy in the ovicidal parasitoid Echthrodelphax fairchildii （Hymenoptera： Dryinidae）

Superparasitism in solitary parasitoids results in fatal competition between the immature parasitoids, and consequently only one individual can emerge. In the semisoli- tary ovicidal parasitoid Echthrodelphaxfairchildii （Hymenoptera： Dryinidae）, 2 adults can emerge under superparasitism with a short interval （〈24 h） between the first and second ovipositions. We determined the female parasitoid＇s behavioral responses under self- and conspecific superparasitism bouts with first-to-second oviposition intervals of 〈2 h. The self- and conspecific superparasitizing frequencies increased up to an oviposition interval of 0.75 h, with the former remaining lower than the latter, particularly for oviposition intervals of _〈0.25 h, suggesting the existence of self-/conspecific discrimination. The superparasitizing frequency plateaued for oviposition intervals of _〉0.75 h, with no dif- ference between self- and conspecific superparasitism. The ovicidal-probing frequency did not differ under self- and conspecific superparasitism, and was usually 〈20%. The females exhibited no preference for the oviposition side （i.e., ovipositing on the side with or without the first progeny） and almost always laid female eggs for any oviposition in- terval under self- and conspecific superparasitism. The sex ratio was not affected by the type of superparasitism, oviposition sides, or the occurrence of ovicidal probing. These observed results about the oviposition side, ovicidal probing, and sex ratios differed from the predictions obtained assuming that the females behave optimally. Possible reasons for the discrepancies are discussed： likely candidates include the high cost of selecting oviposition sides and ovicidal probing, and, for the sex ratio, the low frequency of encountering suitable hosts before superparasitism bouts.     

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.     

Costs and consequences of superparasitism in the polyembryonic parasitoid Copidosoma koehleri (Hymenoptera: Encyrtidae)

Abstract.  1. Polyembryonic wasps provide dramatic examples of intra-specific developmental conflict. In these parasitoids, each egg proliferates into a clonal lineage of genetically identical larvae. If more than one egg is laid in a host (superparasitism), individuals of different clones may compete for food resources.
2. In the polyembryonic encyrtid Copidosoma koehleri , one larva per clone can differentiate into a sterile soldier. It is shown that soldiers are always females, and that they attack intra-specific competitors.
3. Research hypotheses were that (a) clones that develop in superparasitised hosts suffer heavier mortality than clones that develop in singly parasitised hosts, and (b) female clones cause higher mortality to their competitors than male clones, hence larval survival is lower in superparasitised hosts that contain females than in male-only broods.
4. The potential frequency of superparasitism in C. koehleri was manipulated by varying parasitoid–host ratios and exposure durations.
5. As parasitoid densities and exposure durations increased, the frequency of superparasitism rose, brood sizes increased, but the number of hosts that completed development was reduced. The number of offspring per parasitoid female decreased with increasing parasitoid–host ratios. Offspring size and longevity were inversely correlated with brood size. As superparasitism rates increased, fewer all-male broods were produced. Male–female broods were female-biased, suggesting selective killing of males by female soldiers. All-female broods were significantly smaller than all-male broods at high parasitoid densities only, possibly reflecting aggression among soldiers of competing clones.
6. The results support the working hypotheses, and suggest that female larvae outcompete males in superparasitised hosts.     

Patch Exploitation,Patch-leaving and Pre-emptive Patch Defence in the Parasitoid Wasp Trissolcus basalis (Insecta: Scelionidae)

Female parasitoids forage for host resources essential to the development of their offspring, so patch exploitation decisions have a direct influence on their fitness. This paper analyses the patch exploitation behaviour and patch-leaving decisions of the parasitoid wasp Trissolcus basalis (Hymenoptera: Scelionidae), when searching alone on patches of host eggs in the laboratory. Oviposition behaviour was examined in detail and the temporal and sequential structure of patch exploitation was analysed. Time inhomogeneities representing major behavioural change points during patch visits were identified, and the behavioural sequence within homogeneous periods was summarised. As the patch neared full depletion, wasps switched from a repetitive cycle of host examination and oviposition to a ‘leaving routine’, in which they alternated between searching on and off the patch, before abruptly leaving it. Despite the absence of competitors, females remained on the patch for up to 5 h after initiating the leaving routine, and periodically interrupted it to engage in bouts of active patch defence. Such pre-emptive patch defence was more pronounced when the patch was larger and the resource value therefore greater. This unique patch-leaving strategy is interpreted as an adaptation to high levels of resource competition and the consequent risk of losing offspring through superparasitism by competitors.     

Sex allocation and larval competition in a superparasitizing solitary egg parasitoid: competing strategies for an optimal sex ratio

1. Parasitic Hymenoptera reproduce by arrhenotokous parthenogenesis, and females of these species are able to control their progeny sex ratios. In structured populations of parasitic Hymenoptera, primary sex ratios are often highly biased toward females. However, sex ratio can be adjusted to the quality of encountered patches or hosts or be modified by differential developmental mortality.
2. In this paper, the effects were evaluated of the quality of encountered hosts and developmental mortality on the sex ratio in Anaphes victus , a solitary egg parasitoid whose first instar larvae present a sexual dimorphism and where superparasitism is regulated by larval fights between first instar larvae.
3. The results showed that a female-biased sex ratio is allocated to unparasitized hosts. In the presence of parasitized hosts, the second (superparasitizing) female produced a significantly higher sex ratio than the first female but the tertiary sex ratio (sex ratio at emergence) was not significantly different from the sex ratio produced with unparasitized hosts. The increase in the primary sex ratio produced by the second female was mostly compensated by the higher mortality of male larvae.     

Patch exploitation strategy by an egg parasitoid in constant or variable environment

Abstract.  1. In this paper, the foraging behaviour (the proximal mechanisms involved in patch-leaving rules and the egg dispersion) of an egg parasitoid, Anaphes victus , was analysed in environments containing either patches of constant quality (i.e. predictable environment) or patches of variable quality (i.e. unpredictable environment) in order to determine the motivational mechanisms used in patch-leaving strategies.
2. Comparison of the patch exploitation strategy of A. victus between the different habitats suggested that the response of A. victus to a given patch quality strongly depended on its past experiences. Females allocated more time and more eggs in a mixed quality patch after experiencing a poor quality patch than after experiencing a good quality patch. In a poor quality patch, females superparasitised more frequently after experiencing a poor quality patch than after experiencing a good quality patch. In a good quality patch, A. victus females laid more eggs after having visited two poor quality patches than after visiting good quality patches.
3. Recent foraging experiences are used to estimate both the availability and spatial distribution of hosts in the environment and adjust foraging decisions accordingly. The observed variability in the patch-leaving rules within the same species stresses the importance of previous experience when describing behaviours of female parasitoids.     

Patch leaving strategies and superparasitism: an asymmetric generalized war of attrition

When several competitors deplete a patch, it can be advantageous for each of them to stay provided that others leave, whereas, on the other hand, staying longer decreases the expected payoff for everyone. This situation can be considered as a generalized war of attrition. Previous studies have shown that optimal patch leaving strategies become stochastic and the expected leaving time is much larger than predicted by the marginal value theorem when competitors interfere. The possibility of superparasitism, as occurs for example in parasitoids, induces such interference. In addition, it gives several complications. First, the payoff of females that have left the patch is affected by the ovipositions of the remaining individuals. Second, differences in the arrival time of females cause payoff-relevant asymmetries, since females that arrived early on have parasitized more hosts in a patch at the moment superparasitism starts than those that arrived later. We show that this can be modelled as an asymmetric generalized war of attrition, and derive global characteristics of the ESS for simultaneous decisions on when to start superparasitism and when to leave a patch.     

Patch time allocation in male parasitoids

Abstract 1. Patch time allocation has been mostly studied in female parasitoids exploiting patches of hosts. Different parameters such as oviposition, host encounters, patch quality, etc. have been repeatedly shown to modify the time females invest on hosts. 2. Male parasitoids are expected to maximise their lifetime fitness by maximising the number of females inseminated during their life. Because they can be sperm and/or time limited, they should optimise their time allocation on emergence patches. 3. Patch time allocation thus appears to be an important question for both male and female parasitoids. 4. In this study, we determined the parameters used by males of the egg parasitoid Trichogramma turkestanica to decide when to leave the emergence patch. Among the different patch‐leaving parameters tested, only contacts with parasitised hosts and presence of virgin females significantly influenced the patch‐leaving tendency. 5. Our results suggest that males express behaviours that could enable them to optimise their patch exploitation time, as females do, but using different strategies.     

Fitness consequences of superparasitism and mechanism of host discrimination in the stemborer parasitoid Cotesia flavipes

The fitness consequences of superparasitism and the mechanism of host discrimination in Cotesia flavipes, a larval parasitoid of concealed stemborer larvae was investigated. Naive females readily superparasitized and treated the already parasitized host as an unparasitized host by allocating the same amount of eggs as in an unparasitized host. However, there was no significant increase in the number of emerging parasitoids from superparasitized hosts due to substantial mortality of parasitoid offspring in superparasitized hosts. Furthermore, the developmental time of the parasitoids in a superparasitized host was significantly longer than in a singly parasitized host and the emerging progeny were significantly smaller (body length and head width). Naive females entered a tunnel in which the host was parasitized 4 h previously and accepted it for oviposition. Experienced females (oviposition experience in unparasitized host) refused to enter a tunnel with a host parasitized by herself or by another female. In experiments where the tunnel and/or host was manipulated it was demonstrated that the female leaves a mark in the tunnel when she parasitizes a host. The role of patch marking in C. flavipes is discussed in relation to the ecology of the parasitoid.     

Superparasitism as an ESS: to reject or not to reject, that is the question

A stochastic model is formulated to determine the optimal strategy for a solitary parasitoid which has discovered an already parasitized host. The model assumes that the parasitoid can count both the number of eggs already present in a host and the number of conspecifics searching in the same patch. The survival probability of an egg is assumed to depend on the total number of eggs in a host. The decision to (super)parasitize depends both on the degree to which the discovered host already is parasitized and on the number of conspecific females searching in the same patch. We consider both the case that egg laying does not involve any costs for the parasitoid and the case that it involves some marginal costs. Uniform behaviour of all the conspecific parasitoids in a patch, i.e. laying one additional egg in all encountered larvae containing a particular number of eggs, appears to be a pure evolutionary stable strategy (ESS). If either the probability that a parasitoid emerges from a host decreases with an increasing degree of parasitism, at least from a particular number of eggs onwards, or if parasitism involves marginal costs, the maximum number of eggs for which it is still profitable to superparasitize a host once more is limited. This number increases with the number of conspecifics searching in the patch. Large marginal costs (i.e. the expected gain of not parasitizing now) decrease the profit of superparasitism. For newly emerged parasitoids the rejection of an already parasitized host is not advantageous as long as the marginal costs of parasitism are small, because the host can never contain an egg of its own.     

Gamete number and size correlate with adult size in the egg parasitoid Trichogramma euproctidis

In parasitoids, the size of the adult is influenced by the size and quality of the host in which it develops. Body size is generally positively correlated with several adult fitness proxies (fecundity, longevity, and mating capacity). The initial resources available to an individual can influence gamete production (sperm and oocytes), and the number and quality of gametes produced directly influence the expected fitness of both males and females. Gamete production in relation to adult body size was quantified in Trichogramma euproctidis (Girault) (Hymenoptera: Trichogrammatidae), a short‐lived egg parasitoid of lepidopteran species. To avoid host quality variation, male and female parasitoids of different body sizes were produced using superparasitism by allowing mated and virgin female parasitoids to oviposit on Trichoplusia ni Hübner (Lepidoptera: Noctuidae) eggs. Seminal vesicles and ovaries of their offspring were dissected to count oocytes and to measure sperm length and oocytes volume. Tibia length was also measured to estimate body size. The number of oocytes, volume of oocytes, maternal investment index [= (number of oocytes × mean volume of oocytes)/10 000] and sperm length were all significantly positively correlated to body size. These results show that initial resources acquired during larval stage induce phenotypic plasticity in gamete production in both male and female T. euproctidis. Whereas number of sperm and oocytes can influence the fitness of males and females through increased mating capacity and fecundity, variation in gamete size (sperm length and oocyte volume) could also affect the fitness of an individual through sperm and larval competition.     

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.