Gelis Agilis Research Articles

Honeydew composition and its effect on life‐history parameters of hyperparasitoids

1. Diets that maximise life span often differ from diets that maximise reproduction. Animals have therefore evolved advanced foraging strategies to acquire optimal nutrition and maximise their fitness. The free‐living adult females of parasitoid wasps (Hymenoptera) need to balance their search for hosts to reproduce and for carbohydrate resources to feed.2. Honeydew, excreted by phloem‐feeding insects, presents a widely available carbohydrate source in nature that can benefit natural enemies of honeydew‐producing insects. However, the effects of variation in honeydew on organisms in the fourth trophic level, such as hyperparasitoids, are not yet understood.3. This study examined how five different honeydew types influence longevity and fecundity of four hyperparasitoid taxa. Asaphes spp. (Pteromalidae) and Dendrocerus spp. (Megaspilidae) are secondary parasitoids of aphid parasitoids and are thus associated with honeydew‐producing insects. Gelis agilis and Acrolyta nens (both Ichneumonidae) are secondary parasitoids of species that do not use honeydew‐producing hosts.4. Most honeydew types had a positive or neutral effect on life span and fecundity of hyperparasitoids compared with controls without honeydew, although negative effects were also found for both aphid hyperparasitoids. Honeydew produced by aphids feeding on sweet pepper plants was most beneficial for all hyperparasitoid taxa, which can partially be explained by the high amount of honeydew, but also by the composition of dietary sugars in these honeydew types.5. The findings of this study underline the value of aphid honeydew as a carbohydrate resource for fourth‐trophic‐level organisms, not only those associated with honeydew‐producing insects but also ‘interlopers’ without such a natural association.

Reproduction and Offspring Sex Ratios Differ Markedly among Closely Related Hyperparasitoids Living in the Same Microhabitats

Closely related species in nature usually exhibit very similar phylogenetically conserved traits, such as reproduction, behavior and development. Here, we compared fecundity schedules, lifetime reproductive success and offspring sex ratios in three congeneric facultative hyperparasitoid wasps that exhibit several overlapping traits and which co-occur in the same small-scale habitats. Gelis agilis, G. proximus and G. hortensis are abundant in meadows and forest edge habitats in the Netherlands. Gelis agilis is asexual (all female), whereas the other two species reproduce sexually. Here they developed on cocoons of the primary parasitoid Cotesia glomerata. When provided with unlimited hosts, lifetime reproductive success was three times higher in G. proximus than in G. agilis with G. hortensis producing intermediate numbers of offspring. All three species depleted their teneral reserves during their lives. Females of G. proximus and G. hortensis lived significantly longer than females of G. agilis. Offspring sex ratios in young G. proximus mothers were female-biased and marginally male-biased in G. hortensis. As mothers aged, however, the ratio of male:female progeny produced rapidly increased until no daughters emerged later in life. Our results reveal significant differences in reproductive traits among the three species despite them co-occurring in the same microhabitats, being very closely related and morphologically similar. The increase in the production of male progeny by Gelis mothers over time suggests a depletion in sperm number or viability with age. This is especially interesting, given that Gelis species are among the least fecund parasitoids thus far studied. It is likely that in the field most Gelis mothers are probably only able to parasitize a few hosts and to maintain the production of female offspring.

Differential effects of climate warming on reproduction and functional responses on insects in the fourth trophic level

Abstract Understanding the effects of anthropogenic global warming (AGW) on species interactions is essential for predicting community responses to climate change. However, while effects of AGW on resource–consumer interactions at the first and second trophic level have been well studied, little is known about effects on interactions at higher trophic levels at the terminal end of food chains (e.g. in the third and fourth trophic levels). Here, we examined the effects of temperature variability by simulating heatwaves on functional responses of two species at the fourth trophic level (hyperparasitoids) that parasitize host species at the third trophic level (parasitoid cocoons). We found that host cocoons developed faster under simulated heatwave conditions, decreasing the temporal window of susceptibility of the host cocoons to parasitism by the two hyperparasitoids, and consequently parasitism declined with temperature. However, the effects of a simulated heatwave markedly differed among the two hyperparasitoid species; temperature and host quality had a much stronger effect on early reproduction in the less fecund hyperparasitoid Gelis agilis, than in the more fecund species Acrolyta nens. Our results suggest that exposure to heatwaves, that are expected to increase in frequency, will affect the ability of species at higher trophic levels to exploit transient resources whose suitability is temperature‐dependent. In turn, the observed effects of AGW on the functional responses of the hyperparasitoids may disrupt trophic interactions and have profound impact on population dynamics and ecological processes. A plain language summary is available for this article.

Ant-like Traits in Wingless Parasitoids Repel Attack from Wolf Spiders

A recent study showed that a wingless parasitoid, Gelis agilis, exhibits a suite of ant-like traits that repels attack from wolf spiders. When agitated, G. agilis secreted 6-methyl-5-hepten-2-one (sulcatone), which a small number of ant species produce as an alarm/panic pheromone. Here, we tested four Gelis parasitoid species, occurring in the same food chain and microhabitats, for the presence of sulcatone and conducted two-species choice bioassays with wolf spiders to determine their degree of susceptibility to attack. All four Gelis species, including both winged and wingless species, produced sulcatone, whereas a closely related species, Acrolyta nens, and the more distantly related Cotesia glomerata, did not. In two-choice bioassays, spiders overwhelmingly rejected the wingless Gelis species, preferring A. nens and C. glomerata. However, spiders exhibited no preference for either A. nens or G. areator, both of which are winged. Wingless gelines exhibited several ant-like traits, perhaps accounting for the reluctance of spiders to attack them. On the other hand, despite producing sulcatone, the winged G. areator more closely resembles other winged cryptines like A. nens, making it harder for spiders to distinguish between these two species. C. glomerata was also preferred by spiders over A. nens, suggesting that other non-sulcatone producing cryptines nevertheless possess traits that make them less attractive as prey. Phylogenetic reconstruction of the Cryptinae reveals that G. hortensis and G. proximus are ‘sister’species, with G. agilis, and G.areator in particular evolving along more distant trajectories. We discuss the possibility that wingless Gelis species have evolved a suite of ant-like traits as a form, of mimicry to repel predators on the ground.

Honey and honey-based sugars partially affect reproductive trade-offs in parasitoids exhibiting different life-history and reproductive strategies

Adult dietary regimes in insects may affect egg production, fecundity and ultimately fitness. This is especially relevant in parasitoid wasps where many species serve as important biological control agents of agricultural pests. Here, we tested the effect of honey and sugar diets on daily fecundity schedules, lifetime reproductive success and longevity in four species of parasitoid wasps when reared on their respective hosts. The parasitoid species were selected based on dichotomies in host usage strategies and reproductive traits. Gelis agilis and G. areator are idiobiont ecto-parasitoids that develop in non-growing hosts, feed on protein-rich host fluids to maximize reproduction as adults and produce small numbers of large eggs. Meteorus pulchricornis and Microplitis mediator are koinobiont endoparasitoids that develop inside the bodies of growing hosts, do not host-feed, and produce greater numbers of small eggs. Parasitoids were reared on diets of either pure honey (containing trace amounts of proteins), heated honey (with denatured proteins) and a honey-mimic containing sugars only. We hypothesized that the benefits of proteins in honey would enhance reproduction in the ectoparasitoids due to their high metabolic investment per egg, but not in the koinobionts. Pure honey diet resulted in higher lifetime fecundity in G. agilis compared with the honey-mimic, whereas in both koinobionts, reproductive success did not vary significantly with diet. Longevity was less affected by diet in all of the parasitoids, although there were variable trade-offs between host access and longevity in the four species. We argue that there are both trait-based and association-specific effects of supplementary nutrients in honey on reproductive investment and success in parasitoid wasps.

Divergent life history strategies in congeneric hyperparasitoids

Life histories can reveal important information on the performance of individuals within their environment and how that affects evolutionary change. Major trait changes, such as trait decay or loss, may lead to pronounced differences in life history strategies when tight correlations between traits exist. Here, we show that three congeneric hyperparasitoids (Gelis agilis, Gelis acarorum and Gelis areator) that have diverged in wing development and reproductive mode employ markedly different life history strategies. Potential fecundity of Gelis sp. varied, with the wingless G. acarorum maturing a much higher number of eggs throughout life compared with the other two species. Realized lifetime fecundity, in terms of total offspring number was, however, highest for the winged G. areator. The parthenogenic G. agilis invests its resources solely in females, whilst the sexually reproducing species both invested heavily in males to reduce competitive pressures for their female offspring. Longevity also differed between species, as did the direction of the reproduction-longevity trade-off, where reproduction is heavily traded off against longevity only in the asexual G. agilis. Resting metabolic rates also differed between the winged and wingless species, with the highest metabolic rate observed in the winged G. areator. Overall, these geline hyperparasitoids showed considerable divergence in life history strategies, both in terms of timing and investment patterns. Major trait changes observed between closely related species, such as the loss of wings and sexual reproduction, may contribute to the divergence in key life history traits.

Multi-trait mimicry of ants by a parasitoid wasp.

Many animals avoid attack from predators through toxicity or the emission of repellent chemicals. Defensive mimicry has evolved in many species to deceive shared predators, for instance through colouration and other morphological adaptations, but mimicry hardly ever seems to involve multi-trait similarities. Here we report on a wingless parasitoid wasp that exhibits a full spectrum of traits mimicing ants and affording protection against ground-dwelling predators (wolf spiders). In body size, morphology and movement Gelis agilis (Ichneumonidae) is highly similar to the black garden ant (Lasius niger) that shares the same habitat. When threatened, G. agilis also emits a volatile chemical that is similar to an ant-produced chemical that repels spiders. In bioassays with L. niger, G. agilis, G. areator, Cotesia glomerata and Drosophila melanogaster, ants and G. agilis were virtually immune to spider attack, in contrast the other species were not. Volatile characterisation with gas chromatography-mass spectrometry identified G. agilis emissions as 6-methyl-5-hepten-2-one, a known insect defence semiochemical that acts as an alarm pheromone in ants. We argue that multi-trait mimicry, as observed in G. agilis, might be much more common among animals than currently realized.

Host preference and offspring performance are linked in three congeneric hyperparasitoid species

1. The optimisation theory predicts that insect mothers should oviposit on resources on which they attain the highest exclusive fitness. The development of parasitoid wasps is dependent on limited host resources that are often not much larger than the adult parasitoid.2. In the present study preference and development in three congeneric species of secondary hyperparasitoids attacking cocoons of two congeneric primary parasitoids that differ significantly in size were compared. Gelis agilis (Fabricius) and G. acarorum (L.) are wingless hyperparasitoids that forage in grassy habitats, whereas G. areator (Panzer) is fully winged and forages higher in the canopy of forbs.3. The three species were reared on cocoons containing pupae of a small gregarious endoparasitoid, Cotesia glomerata (L.), and a larger solitary species, C. rubecula (Marshall), both of which develop in the caterpillars of pierid butterflies.4. Adult mass was correlated with initial cocoon mass in all three species, whereas development time was unaffected. Wasps were larger when developing in C. rubecula. However, for a given host mass, wasps were larger when developing on the smaller host, C. glomerata. This suggests that there is a physiological limit to hyperparasitoid size that was exceeded when C. rubecula served as host.5. All three hyperparasitoids strongly preferred to attack cocoons of the larger species, C. rubecula, often avoiding cocoons of C. glomerata entirely.6. Preference and performance are correlated in the three Gelis species. However, owing to variation in the distribution and thus abundance of their hosts, it is argued that cumulative fitness may be still higher in the smaller host species.

Parasitoid complex associated with the overwintering generation of Swammerdamia pyrella (Lepidoptera: Yponomeutidae) in Poland.

The study was conducted on fruit trees where bands of corrugated cardboard were attached around the trunks of the trees, which were used to catch the larvae of overwintering generation of the rufous-tipped swammerdamia moth, Swammerdamia pyrella (Villers) (Lepidoptera: Yponomeutidae). Twenty-five species of parasitic Hymenoptera have been described from S. pyrella in Poland including the report in this article of seven species belonging to the family of Ichneumonidae (three species) and superfamily Chalcidoidea (four species). The parasitoids Gelis agilis F. (Ichneumonidae), Chrysocharis aquilegiae (Erdös) (Eulophidae), Catolaccus ater (Ratzeburg) (Pteromalidae), and Eupelmus urozonus (Dalman) (Eupelmidae) had not been reported from the host before. Triclistus pallipes Holmgren (Ichneumonidae), Dibrachys cavus Walker (Pteromalidae) had the greatest effect on the natural regulation of S. pyrella population. Parasitization for the wintering cocoons of S. pyrella changed each year, but it was high throughout the study. The contribution of secondary parasitoids was much higher than primary parasitoids.

Consequences of resource competition for sex allocation and discriminative behaviors in a hyperparasitoid wasp

Population-wide mating patterns can select for equal parental investment in both sexes, but limiting resources, such as mates or developmental substrates, can increase competition leading to biased sex ratios in favor of either sex. Such competition for resources typically occurs in spatially structured populations, where dispersal is limited. In this laboratory study, we investigate if and how resource competition affects sex allocation, discriminative behaviors and competitive interactions of the wingless hyperparasitoid Gelis acororum, which exploits patchily distributed hosts. We show that G. acororum sex ratios are male-biased and that this is not a consequence of constrained reproduction by virgin females. Our results suggest that this pattern of reproductive investment, which is only rarely observed in parasitoids, is a consequence of resource limitation, in terms of hosts rather than mates. Further, G. acororum appears not to respond to intrinsic host quality or to prior oviposition in its host. When competing inter-specifically for host resources, G. acororum outcompetes its congener Gelis agilis, but does so mainly when ovipositing on the host first. Overall, our results suggest that host resource limitation could be an important environmental factor shaping sex allocation in G. acororum, with competition taking place both intra- and inter-specifically.

Parasitoid complex of Zygaena filipendulae L. (Lepidoptera: Zygaenidae)

Caterpillars of Zygaena filipendulae Linnaeus were sampled during May and June in the Sicevo Gorge in southern Serbia. All parasitized larvae were found on grey elm trees (Ulmus canescens). During the short period before metamorphosis of Z. filipendulae, we found the whole specter of parasitoid wasps: Cotesia zygaenarum Marshall (Braconidae), Gelis agilis (Fabricius) and Mesochorus velox Holmgren (Ichneumonidae), Elasmus platyedrae Ferri?re and Pediobius sp. (Eulophidae), Eupelmus vesicularis (Retzius) (Eupelmidae) and Brachymeria tibialis (Walker) (Chalcididae). Beside hymenopteran parasitoids, we found parasitoid flies from the family Tachinidae, Phryxe nemea (Meigen) (Diptera). All 46 observed Z. filipendulae larvae found on grey elm trees were parasitized, but three pupae were found directly on Lotus corniculatus. Two species are newly reported as parasitoids of Z. filipendulae: E. platyedrae and Eupelmus vesicularis and three species (G. agilis, M. velox and E. platyedrae) are new to the fauna of Serbia.

Performance of secondary parasitoids on chemically defended and undefended hosts

Defensive chemicals produced by plants can travel up the food chain by being sequestered by herbivores, and then in turn being sequestered by their parasitoids. Insect species with wide host ranges are predicted to perform poorly in the face of specific chemical defence. However, a species at a high trophic level is expected to have a wide host range. This creates a conflict for hyperparasitoids, many of which depend on specialized hosts. We studied the performance of two hyperparasitoids, Lysibia nana and Gelis agilis, both of which have wide host ranges, on two host species, one chemically defended and the other not. We predicted that both hyperparasitoids would perform better using the undefended host Cotesia glomerata than the defended host C. melitaearum, which sequesters terpenoid allelochemicals (iridoid glycosides). Furthermore, we expected that the progeny of G. agilis collected from an area where hosts defended by iridoid glycosides are absent (the Netherlands) would perform poorly using C. melitaearum in comparison with G. agilis collected from an area where C. melitaearum is a common host (Åland, Finland). In a series of laboratory experiments we found that, contrary to prediction, both hyperparasitoids performed well on both hosts, reaching a larger size on C. glomerata, but having a higher conversion efficiency and developing more quickly on the chemically defended C. melitaearum. Lysibia nana metabolized the plant derived iridoid glycosides, which are chemicals that it does not normally encounter. Gelis agilis retained some of the iridoid glycosides. But whereas Finnish G. agilis retained both aucubin and catalpol, Dutch G. agilis mainly retained aucubin, illustrating that though generalists, local populations still cope differently with toxic allelochemicals.

The effect of different dietary sugars and honey on longevity and fecundity in two hyperparasitoid wasps

In nature adult insects, such as parasitic wasps or ‘parasitoids’ often depend on supplemental nutritional sources, such as sugars and other carbohydrates, to maximize their life-expectancy and reproductive potential. These food resources are commonly obtained from animal secretions or plant exudates, including honeydew, fruit juices and both floral and extra-floral nectar. In addition to exogenous sources of nutrition, adult parasitoids obtain endogenous sources from their hosts through ‘host-feeding’ behavior, whereby blood is imbibed from the host. Resources obtained from the host contain lipids, proteins and sugars that are assumed to enhance longevity and/or fecundity. Here we conducted an experiment exploring the effects of naturally occurring sugars on longevity and fecundity in the solitary hyperparasitoids, Lysibia nana and Gelis agilis. Although both species are closely related, L. nana does not host-feed whereas G. agilis does. In a separate experiment, we compared reproduction and longevity in G. agilis reared on either honey, a honey-sugar ‘mimic’, and glucose. Reproductive success and longevity in both hyperparasitoids varied significantly when fed on different sugars. However, only mannose- and water-fed wasps performed significantly more poorly than wasps fed on four other sugar types. G. agilis females fed honey produced twice as many progeny as those reared on the honey-sugar mimic or on glucose, whereas female longevity was only reduced on the mimic mixture. This result shows not only that host feeding influences reproductive success in G. agilis, but also that non-sugar constituents in honey do. The importance of non-sugar nutrients in honey on parasitoid reproduction is discussed.

Differing Success of Defense Strategies in Two Parasitoid Wasps in Protecting their Pupae Against a Secondary Hyperparasitoid

Abstract During their larval development, endoparasitoids are known to dispose of host resources in several different ways. Some parasitoid wasps consume most or all tissues of the host, whereas others consume a small fraction of host resources and either ensure that the host moves away from the pupation site or allow the host to remain close to the parasitoid cocoon(s). Using a single host species, Mythimna separata Walker (Lepidoptera: Noctuidae), this study compares the success of the two pupation strategies in the solitary parasitoids Microplitis sp. and Meteorus pulchricornis Wesmael (Hymenoptera: Braconidae) against attack from a secondary hyperparasitoid, Gelis agilis F. (Hymenoptera: Ichneumonidae). The caudal appendages of M. separata caterpillars parasitized by Microplitis sp. remain physically attached to parasitoid cocoons and the caterpillars behave aggressively when disturbed. However, after Me. pulchricornis larvae emerge from caterpillars of their host, M. separata, the parasitoid larvae pupate in cocoons that are suspended by a single thick thread that hangs 1–2 cm from under a leaf. In choice tests conducted in petri dishes, significantly fewer cocoons of Microplitis sp. attended by caterpillars than unattended cocoons were hyperparasitized by G. agilis. By contrast, Me. pulchricornis cocoons that were hanging from corn, Zea mays L., plants were hyperparasitized as frequently as those which were attached to leaves. We discuss the potentially different selection pressures generated among natural enemies such as predators and hyperparasitoids in determining optimal pupal defense strategies in primary parasitoids.

The ‘usurpation hypothesis’ revisited: dying caterpillar repels attack from a hyperparasitoid wasp

It has been posited that some parasitoid wasps ‘usurp’ their dying hosts as ‘bodyguards’ to protect the vulnerable parasitoid cocoons against attack from natural enemies such as predators or hyperparasitoids. Thus far, however, the hypothesis has been supported only in studies with insect predators. Two factors may account for this: first, hyperparasitoids, being more specialized than predators, are probably less easily rebuffed by the presence of an attending caterpillar; second, the host cocoon is used for reproduction by hyperparasitoids, but not by predators. We compared the survival of a solitary primary parasitoid, Microplitis sp., and successful parasitism by a secondary hyperparasitoid, Gelis agilis, from parasitoid cocoons with and without the presence of an ‘attending’ larva of the host, the armyworm, Mythimna separata. Mature Microplitis sp. larvae always emerge through the same host segment, leaving the posterior segments paralysed and attached to cocoons and the anterior segments freely moving. When disturbed by G. agilis females, M. separata larvae exhibited aggressive behaviour that repeatedly drove off approaching hyperparasitoids. In choice and no-choice experiments performed at 24 h intervals over 96 h, G. agilis successfully parasitized cocoons without attending caterpillars, but few cocoons with attending caterpillars were ever parasitized. Choice experiments, in which G. agilis wasps were released onto corn plants containing 24 h-old parasitoid cocoons with and without attending caterpillars, produced similar results. We provide the first experimental evidence that a solitary parasitoid usurps the behaviour of its host over several days as a ‘bodyguard’ against hyperparasitoids.

Differing Host Exploitation Efficiencies in Two Hyperparasitoids: When is a 'Match Made in Heaven'?

Host exploitation behavior in two hyperparasitoids, Lysibia nana and Gelis agilis, was compared in single cocoon clusters of their primary parasitoid host, Cotesia glomerata. L. nana reproduces sexually, is fully winged, does not host-feed and matures eggs quite rapidly after eclosion, whereas G. agilis possesses opposite traits. Cohorts of individual hyperparasitoid females of differing age and physiological state were given access to single cocoon clusters of C. glomerata that also varied in age. These results reveal that the reproductive biology of L. nana is well matched to exploit cocoon broods in C. glomerata, suggesting strong a co-evolutionary history with this host. By contrast, G. agilis is much less efficient at exploiting host cocoons and is probably a generalist species that attacks other hosts in nature.

Intrinsic competition between two secondary hyperparasitoids results in temporal trophic switch

Interspecific competition amongst parasitoids is important in shaping the evolution of life-history strategies in these insects as well as community structure. Competition for hosts may occur between adult female parasitoids (‘extrinsic’ competition) or their progeny (‘intrinsic’ competition). Here, we examined intrinsic competition between two solitary secondary hyperparasitoids, Lysibia nana and Gelis agilis in cocoons of a primary parasitoid, Cotesia glomerata. Each species was allowed to sting hosts previously parasitized by the other at 24 h time intervals over the course of 144 h (6 days). When hosts were attacked simultaneously, neither species was dominant although the species to attack first won most encounters when it had a 24–48 h head start. However, after this time there was dramatic shift in the outcome with G. agilis dominating in all hosts > 72-h old, regardless of which species had parasitized C. glomerata first. G. agilis larvae, which initially had competed with L. nana for control of C. glomerata resources, began attacking the larvae of L. nana, whereas L. nana rejected hosts with older G. agilis larvae or pupae. Effects of multiparasitism also affected the development time and adult mass of the winning parasitoid. Our results reveal a shift in the trophic status of G. agilis from C. glomerata (in younger hosts) to L. nana (in older hosts), the first time such a phenomenon has been reported in parasitoids.

Interactions to the fifth trophic level: secondary and tertiary parasitoid wasps show extraordinary efficiency in utilizing host resources

1. Parasitoid wasps are highly efficient organisms at utilizing and assimilating limited resources from their hosts. This study explores interactions over three trophic levels, from the third (primary parasitoid) to the fourth (secondary parasitoid) and terminating in the fifth (tertiary parasitoid). 2. Host utilization and adult body mass of the secondary and tertiary parasitoid Gelis agilis was determined when developing on pre-pupae of its primary parasitoid host, Cotesia glomerata, and from pre-pupae of another secondary parasitoid, Lysibia nana that had developed initially on pre-pupae of C. glomerata. 3. In both C. glomerata and G. agilis, the body mass of emerging adult parasitoids was strongly positively correlated with initial cocoon mass. For a given cocoon mass at parasitism, emerging adult G. agilis wasps were almost 90% as large as C. glomerata adults developing in healthy cocoons of comparable mass. Furthermore, G. agilis adults were still 75% as large as C. glomerata adults even when developing on L. nana that in turn had developed on C. glomerata. Otherwise, in terms of adult body mass per unit of host resources, there was no apparent difference in the quality of C. glomerata or L. nana hosts for the development of G. agilis. 4. Analyses of carbon and nitrogen in body tissues of the parasitoids over the third to the fifth trophic level revealed that percentage nitrogen was higher and carbon lower in G. agilis and L. nana than in C. glomerata. Furthermore, percentage carbon was lower in adult G. agilis wasps that had developed from L. nana than from C. glomerata. 5. We argue that the remarkable efficiency which characterizes the development of secondary and tertiary parasitoids is based on the very high nutritional quality of resources that increase in quality up the food chain and rigid selection optimizing allocation of limited host resources. Consequently, food webs involving secondary and tertiary parasitoids can go to levels hitherto unexplored thus far in empirical studies. The use of molecular markers in future studies may reveal just how long food chains involving these insects may extend.

Comparing and contrasting development and reproductive strategies in the pupal hyperparasitoids Lysibia nana and Gelis agilis (Hymenoptera: Ichneumonidae)

In most animals, the optimal phenotype is determined by trade-offs in life-history traits. Here, I compare development and reproductive strategies in two species of solitary secondary hyperparasitoids, Lysibia nana and Gelis agilis, attacking pre-pupae of their primary parasitoid host, Cotesia glomerata. Parasitoid larvae of both species exploit a given amount of host resources with similar efficiency. However, adults exhibit quite different reproductive strategies. Both species are synovigenic, and female wasps emerge with no mature eggs. However, G. agilis must first host-feed to produce eggs, while L. nana does not host-feed but mobilizes internal resources carried over from larval feeding to initiate oogenesis. Further, G. agilis is wingless, produces large eggs, has a long life-span, and generates only small numbers of progeny per day, whereas these traits are reversed in L. nana. Given unlimited hosts, the fecundity curve in L. nana was “front-loaded,” whereas in G. agilis it was depressed and extended over much of adult life. In L. nana (but not G. agilis), wasps provided with honey but no hosts lived significantly longer than wasps provided with both honey and hosts. Differences in the fecundity curves of the two hyperparasitoids are probably based on differing costs of reproduction between them, with the wingless G. agilis much more constrained in finding hosts than the winged L. nana. Importantly, L. nana is known to be a specialist hyperparasitoid of gregarious Cotesia species that pupate in exposed locations on the food plant, whereas Gelis sp. attack and develop in divergent hosts such as parasitoid cocoons, moth pupae and spider egg sacs. Consequently, there is a strong match between brood size in C. glomerata and egg production in L. nana, but a mismatch between these parameters in G. agilis.

The parasitoid complex associated with the herbivore Hadena bicruris (Lepidoptera: Noctuidae) on Silene latifolia (Caryophyllaceae) in the Netherlands

Larvae of the moth, Hadena bicruris, constitute the most important predispersal seed predator on Silene latifolia (Caryophyllaceae). Parasitoids attacking the larvae of this specialist noctuid can potentially decrease the amount of damage to the plant. This paper describes and quantifies the parasitoid complex associated with H. bicruris in the Netherlands, and documents life history characters of its species. Forty‐four percent of larval H. bicruris were parasitized by at least 13 species of parasitoids. The most prevalent of these were the braconids Microplitis tristis (22.9%) and Bracon variator (4.9%) and the ichneumonids Eurylabus tristis (11.7%) and Ophion pteridis (3.4%). Other species occurring sporadically were: the ichneumonids Scambus brevicornis, S. buolianae, Erigorgus cerinops, and Hyposoter sp.; the tachinids Phryxe vulgaris, P. nemea, Blondelia nigripes and Siphona geniculata; and a Mermithidae sp. The ichneumonid hyperparasitoid Mesochorus lanceolatus was found occasionally in larvae of M. tristis. The hyperparasitoid ichneumonids Gelis agilis, G. hortensis and the chalcids Baryscapus endemus, Pteromalus chrysos and P. vibulenus were found in cocoons of both M. tristis and B. variator. The primary parasitoids M. tristis, E. tristis, and to a lesser extent, O. pteridis, are believed to be specialized on Hadena. The effect of the parasitoids on herbivory by their host is probably small because the most common parasitoid species are koinobionts that attack large, late instar hosts. Only B. variator and Scambus spp., which are ectoparasitoids, arrest host development immediately upon parasitism, but like the other parasitoids they kill mainly large L4 or L5 hosts. The gregarious M. tristis and B. variator produce clutches with a female‐biased sex ratio, in contrast to the solitary E. tristis where the sex ratio approaches equality. The ectoparasitoid B. variator produces mostly single‐sex clutches, probably avoiding deleterious effects of inbreeding. The clutch size distributions suggest that large clutches of M. tristis and B. variator are probably caused by multiple parasitisms.