Apostolos Kapranas

Sequences of sex allocation and mortality in clutches of Metaphycus parasitoids of soft scale insects and the prevalence of all-female broods.

1. In many gregarious or quasi‐gregarious parasitoids that experience local mate competition, precise sex ratios with low variance are observed. Precise sex ratios can be achieved by laying male and female eggs in non‐random sequences.

Larval cannibalism during the late developmental stages of a facultatively gregarious encyrtid endoparasitoid

1 The larvae of many gregarious parasitoid species are usually non‐aggressive when they develop in or on a host, but those of Metaphycus flavus are one of the few exceptions known. Herein we describe their aggressive behaviour and the conditions under which it occurs, using observations in which larval development and physical conflict within parasitised and superparasitised hosts were mapped daily. 2 Metaphycus flavus larvae often engaged in physical conflict that resulted in consumption of the losing larvae (= cannibalism ) in superparasitised hosts, whereas such conflict and consumption occurred rarely when a single brood developed in a host. 3 Cannibalism among M. flavus larvae only occurred after the host resources had become scarce. Typically it occurred after the sixth day of development (fourth‐instar larvae) when the larvae in a clutch had separated from their aeroscopic plate and were freed of their attachment to the hosts cuticle. 4 Female larvae in the initial clutch appeared more aggressive than male larvae when a second clutch was allocated 4 h after the first clutch. The probability of a larva being attacked and consumed by a brood mate increased as the number of larvae increased in the host. This partial tolerance might allow the members of the initial brood to defend themselves from offspring of a superparasitising female (= competitors ). Such post‐ovipositional regulation of brood size might be interpreted as high‐density intolerance among female offspring.

Mutually beneficial host exploitation and ultra-biased sex ratios in quasisocial parasitoids

Selfish interests usually preclude resource sharing, but under some conditions collective actions enhance per capita gains. Such Allee effects underlay early explanations of social evolution but current understanding focusses on kin selection (inclusive fitness). We find an Allee effect that explains unusual quasisociality (cooperative brood care) among parasitoid wasps without invoking or precluding kin selection effects. In Sclerodermus harmandi, individual females produce most offspring when exploiting small hosts alone. However, larger hosts are more successfully exploited by larger groups of females, with the per-female benefits outweighing the costs of host sharing. Further, the extremely biased sex ratios (97% female) are better explained by mutually beneficial female–female interactions that increase the reproductive value of daughters (local resource enhancement), rather than by the usually invoked local mate competition between males. Thus, atypical quasisocial behaviour in a parasitoid wasp directly enhances reproductive success and selects for very extremely female-biased sex ratios.

Higher relatedness mitigates mortality in a nematode with lethal male fighting

According to kin selection theory, individuals show less aggression towards their relatives. Limited dispersal promotes interactions among relatives but also increases competition among them. The evolution of cooperation in viscous populations has been subject of mainly theoretical exploration. We investigated the influence of relatedness on aggression in males of entomopathogenic nematode Steinernema longicaudum that engage in lethal fighting. In a series of in vitro experiments, we found that both competitor male group size and relatedness influence male mortality rates. Higher relatedness led to progressively lower rates of male mortality. In experimentally infected insects, wherein large numbers of males and females interact, the proportion of dead and paralysed (= terminally injured) males was higher when infection was established by infective juveniles originating from a mixture of three lines than in those infected by a single line. The results collectively show that Steinernema longicaudum males recognize their kin and consequently male mortality rates are lower in groups consisting of more related males. Furthermore, this monotonic negative relationship between aggression and relatedness suggests that kin selection benefits are still substantial even under extreme competition. Our experiments also suggest that kin recognition in entomopathogenic nematodes has a genetic basis rather than being strictly based on environmental cues. We discuss our findings within the theoretical context of the evolution of altruistic/cooperative behaviour in structured populations.

Encyrtid Parasitoids of Soft Scale Insects: Biology, Behavior, and Their Use in Biological Control

Parasitoids of the hymenopterous family Encyrtidae are one of the most important groups of natural enemies of soft scale insects and have been used extensively in biological control. We summarize existing knowledge of the biology, ecology, and behavior of these parasitoids and how it relates to biological control. Soft scale stage/size and phenology are important determinants of host range and host utilization, which are key aspects in understanding how control by these parasitoids is exerted. Furthermore, the nutritional ecology of encyrtids and their physiological interactions with their hosts affect soft scale insect population dynamics. Lastly, the interactions among encyrtids, heteronomous parasitoids, and ants shape parasitoid species complexes and consequently have a direct impact on the biological control of soft scale insects.

Metabolomics of aging assessed in individual parasitoid wasps.

Metabolomics studies of low-biomass organisms, such as small insects, have previously relied on the pooling of biological samples to overcome detection limits, particularly using NMR. We show that the differentiation of metabolite profiles of individual 1 mg parasitoid wasps of different ages is possible when using a modified sample preparation and a combination of untargeted NMR and LC-MS based metabolomics. Changes were observed between newly emerged and older wasps in glycerolipids, amino acids and circulatory sugars. This advance in chemical profiling has important implications for the study of the behaviour and ecology of parasitoids and many other species of small organisms because predictions and observations are typically made at the level of the individual. Thus, the metabolomic state of low-biomass individuals can now be related to their behaviour and ecological performance. We discuss specifically the utility of age-related metabolomic profiling but our new approach can be applied to a wide range of biological research.

Sex ratios, virginity and local resource enhancement in a quasisocial parasitoid

Sclerodermus harmandi (Buysson) (Hymenoptera: Bethylidae) is an economically beneficial species of parasitoid wasp that has an unusual level of sociality: groups of female foundresses reproduce on a single host and exhibit cooperative post‐ovipositional brood care. The beneficial effects females have on each others reproductive success provide, via the theory of local resource enhancement (LRE), an explanation for their female‐biased progeny sex ratios, which is part of the same framework for understanding sex‐ratio evolution as the more often invoked theory of local mate competition (LMC). Here, we show that S. harmandi sex ratios are overdispersed, with high variance largely attributable to the common occurrence (60%) of developmental mortality. Developmental mortality is also positively associated with the proportion of broods which contain only females at emergence (virgin broods). Virginity is more common when broods are produced by fewer foundresses. Virginity is expected to be disadvantageous under LRE, as it is under LMC, but theory for LRE is less extensively developed. We suggest approaches for the development of LRE theory, in particular using models of ‘population elasticity’ in which the intensity of kin competition is reduced because extra resources are available to local populations that are more cooperative. For S. harmandi, such extra resources may include large hosts that can only be successfully utilised if multiple foundresses cooperate.

Larval morphology of Metaphycus flavus and its role in host attachment and larval cannibalism

Metaphycus flavus (Howard) (Hymenoptera: Encyrtidae) is a facultatively gregarious endoparasitoid of soft scales (Hemiptera: Coccidae). When it develops in superparasitised hosts, the larvae often attack and consume brood mates six or more days post oviposition. Under our laboratory conditions (25±1°C and 14 hours of light followed by 18±1°C and ten hours of darkness in 50-70% R.H.), M. flavus eggs hatched three days after oviposition. Measurements of the mandibles and tentorium indicate there are four larval instars, and M. flavus reaches the fourth instar by day six post oviposition, and pupates on day eight. Thus, cannibalism among M. flavus larvae occurs during the fourth instar. During this instar, M. flavus larvae separate from their attachment to the scale cuticle, to which they were tethered by a respiratory structure during the previous three larval instars. Once detached, they are free to move within the scale, which increases the probability of larval encounters and aggressive behaviours. Moreover, the mandibles of the fourth instar are better adapted for fighting than are those of the first three larval instars, since they are larger and more sclerotized. The cranium and mouthparts of M. flavus have four different types of sensory organs, some of which are almost certainly olfactory, an unexpected function for a larva that presumably is surrounded by an aqueous medium where gustatory sensilla would seem to be more appropriate. The cranium also bears two pairs of what appear to be secretory pores.

Reproductive efficiency of the bethylid wasp Cephalonomia tarsalis: the influences of spatial structure and host density

The parasitoid wasp Cephalonomia tarsalis (Ashmead) (Hymenoptera: Bethylidae) is commonly present in stored product facilities. While beneficial, it does not provide a high degree of biological pest control against its host, the saw-toothed beetle Oryzaephilus surinamensis (L.) (Coleoptera: Silvanidae). A candidate explanation for poor host population suppression is that adult females interfere with each others foraging and reproductive behavior. We used simple laboratory microcosms to evaluate such mutual interference in terms of its overall effects on offspring production. We varied the density of the hosts and also the spatial structure of the environment, via the extent of population sub-division and the provision of different substrates. Production of C. tarsalis offspring was positively influenced by host density and by the isolation of females. With incomplete sub-division within microcosms offspring production was, in contrast, low and even zero. The provision of corrugated paper as a substrate enhanced offspring production and partially mitigated the effects of mutual interference. We recommend simple improvements to mass rearing practice and identify promising areas for further behavioral and chemical studies towards a better understanding of the mechanisms of mutual interference.

Optimizing the application method of entomopathogenic nematode suspension for biological control of large pine weevil Hylobius abietis

Entomopathogenic nematodes (EPNs) are effective against the immature stages of the large pine weevil Hylobius abietis. In three field trials we compared the efficacy of the application method of EPN for weevil suppression below the suggested threshold of 20 weevils per stump: applying the EPN suspension in the top edges of the stumps (‘top’) vs. drenching the soil around stumps (‘standard’). For Steinernema carpocapsae, weevil suppression was below the targeted threshold only when suspension was applied in the standard way (two of the three sites). On the other hand, weevil suppression was provided in all three cases of ‘top’ application of Heterorhabditis downesi suspension, whereas suppression in ‘standard’ application was observed in one site. Percentage parasitism of developing weevils in relation to depth and distance help explain EPN movement post-application. Weevil suppression relative to suggested thresholds can be improved by altering the method of EPN application depending on the nematode species.