Parasitoids update the habitat profitability by adjusting the kairomone responsiveness to their oviposition experience

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Stage-specific sex differences in Drosophila immunity to parasites and pathogens

Arguments from life-history theory predict that other things being equal females are likely to invest more in defence against parasites and pathogens than males. This is either because males and females differ in behaviour or, more importantly, because the variance in mating success is typically higher in males than in females. Such effects are likely to be most pronounced in those developmental stages where sex differences are greatest. In most organisms, but especially in holometabolous insects, this will be the adult stage. We explored sex-specific resistance to four natural enemies of Drosophila melanogaster that attack the insect at different developmental stages: the larval parasitoid Asobara tabida, the pupal parasitoid Pachycrepoideus vindemiae; and the adult pathogens Beauvaria bassiana (a fungus) and Tubulinosema kingi (a microsporidian). Measures of resistance were designed to reflect the four species’ natural history. Female larvae were able to defend themselves more strongly against A. tabida than males and there was weak evidence that adult females suffered less from microsporidian attack than males. No differences were found for the other two species. Our results provide some support for lower investment in defences in males, and we discuss why the strongest effect was found at the larval rather than the adult stage contrary to our prediction.     

Knowing your habitat: linking patch-encounter rate and patch exploitation in parasitoids

According to optimal foraging theory, animals should decidewhether or not to leave a resource patch by comparing the currentprofitability of the patch with the expected profitability ofsearching elsewhere in the habitat. Although there is abundantevidence in the literature that foragers in general are wellable to estimate the value of a single resource patch, theirdecision making has rarely been investigated with respect tohabitat quality. This is especially true for invertebrates.We have conducted experiments to test whether parasitic waspsadjust patch residence time and exploitation in relation tothe abundance of patches within the environment. We used thebraconid Asobara tabida, a parasitoid of Drosophila larvae,as our model species. Our experiments show that these waspsreduce both the residence time and the degree of patch exploitationwhen patches become abundant in their environment, as predictedby optimal foraging models. Based upon a detailed analysis ofwasp foraging behavior, we discuss proximate mechanisms thatmight lead to the observed response. We suggest that parasitoidsuse a mechanism of sensitization and desensitization to chemicalsassociated with hosts and patches, in order to respond adaptivelyto the abundance of patches within their environment.     

When Parasitoid Males Make Decisions: Information Used when Foraging for Females

Optimal foraging models predict how an organism allocates its time and energy while foraging for aggregated resources. These models have been successfully applied to organisms such as predators looking for prey, female parasitoids looking for hosts, or herbivorous searching for food. In this study, information use and patch time allocation were investigated using male parasitoids looking for mates. The influence of the former presence of females in absence of mates and the occurrence of mating and other reproductive behaviours on the patch leaving tendency was investigated for the larval parasitoid Asobara tabida. Although males do not modify their patch residence time based on the number of females that visited the patch, they do show an increase in the patch residence time after mating a virgin female and performing courtship behaviour such as opening their wings. These results are in concordance with an incremental mechanism, as it has been described for females of the same species while foraging for hosts. The similarities between males and females of the same species, and the conditions under which such a patch-leaving decision rule is fitted are discussed. This is the first study describing an incremental effect of mating on patch residence time in males, thus suggesting that similar information use are probably driving different organisms foraging for resource, regardless of its nature.     

Host preference and survival in selected lines of a Drosophila parasitoid,Asobara tabida

Host selection behaviour of parasitoids has important fitness consequences, if hosts of different quality are available. Here the host selection behaviour, the ability to distinguish between hosts differing in their suitability, of the Drosophila parasitizing wasp Asobara tabida was studied. Females from five lines selected for higher survival in the encapsulating host species D. melanogaster ( 16 ) were compared with females from control lines. Females from all five selected lines more readily accepted the encapsulating host species for oviposition when offered together with a nonencapsulating host species than females from the control lines. We found no evidence for pleiotropic effects and suggest that host selection behaviour evolved parallel to the ability to escape encapsulation in the hosts. Our results also suggest that given the appropriate selection pressures, host selection behaviour can quickly evolve in parasitoids, enabling them to adapt fast to changing circumstances.     

Patch choice from a distance and use of habitat information during foraging by the parasitoid Ibalia leucospoides

1. In environments in which resources are distributed heterogeneously, patch choice and the length of time spent on a patch by foragers are subject to strong selective pressures. This is particularly true for parasitoids because their host foraging success translates directly into individual fitness. 2. The aim of this study was to test whether: (i) females of the parasitoid Ibalia leucospoides (Hymenoptera: Ibaliidae) can discriminate among patches according to host numbers; (ii) the surrounding context affects the initial choice of patch, as well as time spent on patch; and (iii) the perceived quality of a given patch is affected by the quality of the surrounding patches. 3. Each female was randomly exposed to one of three different three‐patch environments which differed in host number per patch, mean environment host number and host distribution among patches. For each treatment level, the first patch chosen and the time allocated to each patch visited by the female were recorded. 4. Females of I. leucospoides were able to discriminate different levels of host numbers among patches from a distance. The patch bearing the highest number of hosts was, predominantly, the first choice. Patch host number in association with mean habitat profitability influenced the length of time spent on the first patch visited. By contrast, variance in habitat profitability did not influence time allocation decisions. Contrary to the study prediction, there were no significant habitat‐dependent time allocation differences among patches holding the same number of hosts. 5. The results indicate that, for I. leucospoides, patch exploitation decisions are partially influenced by information obtained from the habitat as a whole, a behaviour that may prove to indicate adaptive ability in highly patchy environments, as well as suggesting the presence of good cognitive abilities in this parasitoid species.     

Geographic variation in reproductive success of the parasitoid Asobara tabida in larvae of several Drosophila species

Abstract.

• 1 Asobara tabida is a parasitoid of Drosophila larvae in fermenting substrates. Because it is a widespread species, it may encounter different biotic and abiotic circumstances in various parts of its range.
• 2 The species composition of the host population varies over the parasitoid's range: D.obscura-group species (especially D.subobscura) are the main hosts for northwestern and central European parasitoids; D.melanogaster is the main host for southern European parasitoids.
• 3 D.melanogaster larvae can defend themselves against A.tabida by encapsulating the parasitoid egg, and survival in D.melanogaster is always lower than in D.subobscura.
• 4 Parasitoids from southern European populations are much better able to survive in D.melanogaster than their northwestern and central European conspecifics; parasitoids from different populations are equally well able to survive in D.subobscura.
• 5 The lower survival in D.melanogaster may be partly compensated for by the larger size of parasitoids emerging from this host species compared to parasitoids emerging from D.subobscura.
• 6 Within population groups, larger A.tabida females have more eggs in their ovarioles. Additionally, southern European females have more eggs and less fat than northern and western/central European females. The relationship between size and longevity is ambiguous.
• 7 It is concluded that parasitoids from different populations are adapted to region-specific circumstances.

     

Kleptoparasitism as an explanation for paradoxical oviposition decisions of the parasitoid Asobara tabida

It is known that the braconid Asobara tabida, a parasitoid of Drosophila larvae, takes oviposition decisions in accordance with survival probabilities in several host species. Nevertheless, larvae of D. simulans, in which the survival probability is virtually zero, are readily accepted for oviposition by searching females. This even happens when they are offered together with D. melanogaster larvae, in which the parasitoid can develop. Here I show that A. tabida can act as a kleptoparasitoid in D. simulans larvae: it can develop in D. simulans larvae, once these larvae are parasitized by another parasitoid, the eucoilid Leptopilina boulardi. Analysis with an optimal foraging model suggests that the increase in survival probability and the occurrence of L. boulardi in the field are high enough to make this kleptoparasitic behaviour of A. tabida pay.     

Oviposition behavior ofDrosophila subobscura and its parasitoidAsobara tabida in the laboratory

At 18°C, adultAsobara tabida emerge 21 days after oviposition within the host;Drosophila subobscura emerges 18 days after oviposition. The relatively short pre-oviposition period of adultA. tabida (4 days), compared to that ofD. subobscura (4–8 days) results in the generation times of both host and parasitoid being approximately similar. A yeast source is necessary forD. subobscura females to mature their eggs; female flies will not oviposit on patches without a yeast source. While surface roughness is an important characteristic for maximumD. subobscura oviposition,A. tabida oviposition, and consequent levels of parasitism, is enhanced by coating patches with askin of active yeast. When presented with a multi-patch environment, experienced and inexperienced female wasps showed no significant difference in their level of attack.     

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.     

Effects of parasitism by Asobara tabida (Hymenoptera: Braconidae) on the development,survival and activity of Drosophila melanogaster larvae

The impact of parasitism by Asobara tabida on Drosophila melanogaster larval development, survival features and larval activity has been investigated using two strains of the parasitoid. The successful parasitism rate of the A1 strain was four times greater than that of the WOPV strain. Both strains induced equivalent mortality rates but hosts parasitized by A1 predominantly died as pupae. The time necessary for the host pupariation and emergence, and the larval weight at 72, 96 and 120 h post-parasitization were measured. Parasitized larvae exhibited longer periods of development and lower weights than controls, especially when parasitized by A1. These results suggest that hosts underwent physiological costs varying with respect to the outcome of the parasitic relationship. Of the parasitoid factors possibly responsible for these costs, we examined venoms for their impact on host mortality. Artificial injections of WOPV venoms induced higher mortality rates than did A1 venoms. Venoms were also found responsible for the induction of a transient paralysis, naturally occuring after parasitization. Again, the strongest effect was observed after parasitization by WOPV or injections of its venoms. This study gives new insights into the intriguing features of A. tabida and constitutes the first report of the paralysing properties of the venoms.     

Effect of host deprivation on the foraging behavior of the Asian citrus psyllid parasitoid Tamarixia radiata: observations from the laboratory and the field

The Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), is a significant citrus pest and the parasitoid Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) has been released in various citrus‐producing areas in classical biological control programs targeting D. citri. We investigated the effect of host deprivation on the foraging behavior and patch utilization by T. radiata. In the laboratory, females deprived of hosts for 3 days tended to leave patches of 12 nymphs without parasitizing hosts during the ca. 30 min they spent in the patch before leaving. Moreover, half of these females failed to host feed, and those that did host feed, on average, needed more than 15 min to complete feeding. Conversely, non‐host‐deprived females parasitized on average three nymphs before leaving patches without host feeding during the ca. 39 min they spent in the patch. These laboratory observations were compared to mass‐reared female T. radiata that were released onto colonies of D. citri nymphs infesting citrus in the field. Release vials were provisioned with honey and these females had no opportunities to host feed over the 1‐ to 2‐day containment period prior to release. When introduced onto D. citri colonies, 68% T. radiata females abandoned D. citri patches prior to probing hosts, in part, because Argentine ants, Linepithema humile (Mayr) (Hymenoptera: Formicidae), tending colonies disturbed searching parasitoids. These results from laboratory and field studies are discussed in the context of classical biological control, with the aim of understanding how to manipulate host availability and ant activity so establishment rates and impact of T. radiata can be improved.     

Intra- and interspecific host discrimination in Asobara (Hymenoptera) larval endo-parasitoids of Drosophilidae: Comparison between closely related and less closely related species

Host discrimination studies were conducted with different species of Asobara, which are larval endo-parasitoids of Drosophilidae. Results indicated variable host discrimination which depended on the relatedness of the species. The closely related sibling species Asobara tabida (Nees) and A. rufescens (Foerster) were not only capable of intraspecific discrimination, but also avoided multiparasitism by discriminating between unparasitized host larvae and larvae previously parasitized by females of the other species. This ability to discriminate interspecifically does not seem functional as each species occupies its own microhabitat. As it was shown to be absent in less closely related Asobara species we concluded that interspecific discrimination by A. tabida and A. rufescens was due to their close relationship.     

Response of life‐history traits to artificial and natural selection for virulence and nonvirulence in a Drosophila parastitoid,Asobara tabida

Co‐evolution of host–parasitoid interactions is determined by the costs of host resistance, which received empirical evidence, and the costs of parasitoid virulence, which have been mostly hypothesized. Asobara tabida is a parasitoid, which mainly parasitizes Drosophila melanogaster and D. subobscura, the first species being able to resist to the parasitoid development while the second species is not. To parasitize resistant hosts, including D. melanogaster, A. tabida develops sticky eggs, which prevent encapsulation, but this virulence mechanism may be costly. Interindividual and interpopulation variation in the proportion of sticky eggs respectively allowed us to (i) artificially select and compare life‐history traits of a virulent and a nonvirulent laboratory strain, and (ii) compare a virulent and a nonvirulent field strain, to investigate the hypothetical costs of virulence. We observed strong differences between the 2 laboratory strains. The nonvirulent strain invested fewer resources in reproduction and walked less than the virulent one but lived longer. Concerning the field strains, we observed that the nonvirulent strain had larger wings while the virulent one walked more and faster. All together, our results suggest that virulence may not always be costly, but rather that different life histories associated with different levels of virulence may coexist at both intra‐ and interpopulation levels.     

Nectar provisioning close to host patches increases parasitoid recruitment,retention and host parasitism

In the adult stage, many parasitoids require hosts for their offspring growth and plant-derived food for their survival and metabolic needs. In agricultural fields, nectar provisioning can enhance biological control by increasing the longevity and fecundity of many species of parasitoids. Provided in a host patch, nectar can also increase patch quality for parasitoids and affect their foraging decisions, patch time residence, patch preference or offspring allocation. The aim of this study was to investigate the impact of extrafloral nectar (EFN) provisioning close to hosts on parasitoid aggregation in patches. The aphid parasitoid Diaeretiella rapae (M’Intosh) was released inside or outside patches containing Brassica napus L. infested by Brevicoryne brassicae L. aphids and Vicia faba L. with or without EFN. When parasitoids were released outside patches, more parasitoids were observed in patches with EFN than in patches deprived of EFN. This higher recruitment could be linked to a higher attraction of a combination of host and food stimuli or a learning process. A release–recapture experiment of labeled parasitoids released within patches showed the higher retention of parasitoids in patches providing EFN and hosts, suggesting that food close to the host patch affects patch residence time. Both attractiveness and patch retention could be involved in the higher number of parasitoids foraging in host patches surrounded by nectar and for the higher parasitism recorded. Nectar provisioning in host patches also affected female offspring allocation inside the patch.     

Interspecific interference between Apoanagyrus lopezi and A. diversicornis, parasitoids of the cassava mealybug Phenacoccus manihoti

The parasitoids Apoanagyrus lopezi De Santis and A. diversicornis (Howard) (Hymenoptera: Encyrtidae) have been introduced into Africa for the biological control of the cassava mealybug Phenacoccus manihoti Matile-Ferrero (Homoptera: Pseudococcidae). We have studied competition between these species to investigate if they can coexist. Here we report on the influence of the simultaneous presence of non-conspecific adult females on searching efficiency on patches. Wasps of either species foraged on discs of cassava leaf with mealybugs, while at the same time different numbers of non-conspecifics were also depleting the patch. Patch area per parasitoid and number of hosts available to each parasitoid were equal in all treatments.In both species, the presence of other foragers clearly affected several aspects of the parasitoids' behaviour. Patch residence time increased with the number of non-conspecifics in A. diversicornis. In both parasitoid species, the proportion of hosts left unparasitized after the patch visit decreased with increasing numbers of females on the patch. The proportions of super- and multiparasitism did not change with the number of females. Both species produced more offspring during a patch visit in the presence of more non-conspecifics. These behavioural changes did not, however, lead to a change in the offspring production rate on patches. A. diversicornis produced offspring at a rate three times that of A. lopezi when one A. lopezi and one A. diversicornis foraged simultaneously. This is the first report of an aspect of interspecific competition where A. diversicornis has an advantage over A. lopezi. Interference between adult females thus promotes coexistence of the two species on P. manihoti.     

Host–parasitoid interaction as affected by interkingdom competition

Although still underrepresented in ecological research, competitive interactions between distantly related organisms (so-called “interkingdom competition”) are expected to be widespread in various ecosystems, with yet unknown consequences for, e.g. trophic interactions. In the model host–parasitoid system Drosophila melanogaster–Asobara tabida, toxic filamentous fungi have been shown to be serious competitors that critically affect the density-dependent survival of host Drosophila larvae. This study investigates the extent to which the competing mould Aspergillus niger affects key properties of the well-studied Drosophila–parasitoid system and how the host–parasitoid interaction influences the microbial competitor. In contrast to slightly positive density-dependent host mortality under mould-free conditions, competing A. niger mediated a strong Allee effect for parasitised larvae, i.e. mortality decreased with increasing larval density. It was found that the common toxic fungal metabolite kojic acid is not responsible for higher death rates in parasitised larvae. Single parasitised Drosophila larvae were less harmful to fungal reproduction than unparasitised larvae, but this effect vanished with an increase in larval density. As predicted from the negative effect of fungi on host survival and thus on parasitoid fitness at low larval densities, A. tabida females spent less time foraging in fungus-infested patches. Interestingly, even though high host larval densities increased host survival, parasitoids still reduced their search efforts in fungus-infested patches, indicating a benefit for host larvae from feeding in the presence of noxious mould. Thus, this experimental study provides evidence of the potentially important role of interkingdom competition in determining trophic interactions in saprophagous animal communities and the dynamics of both host–parasitoid and microbial populations.     

The oviposition behavior ofAphidius ervi andMonoctonus paulensis (Hymenoptera: Aphididae) encountering different host species (Homoptera: Aphididae) in sequential patches

Two-day-old mated females ofAphidius ervi Haliday andMonoctonus paulensis (Ashmead) were each provided with two sequential host patches. Patches were comprised of plastic petri dishes containing either 15 pea aphids,Acyrthosiphum pisum (Harris), or 15 alfalfa aphids,Macrosiphum creelii Davis. Both wasp species parasitized more hosts in patches containing pea aphids than in those containing alfalfa aphids, regardless of sequence. Females ofA. ervi also laid more eggs per aphid in patches containing pea aphids than in patches containing alfalfa aphids. When both patches contained alfalfa aphids,M. paulensis females parsitized more aphids in the second patch than in the first. Fewer alfalfa aphids were parasitized in the second patch when the first patch contained pea aphids, and fewer eggs were laid per alfalfa aphid. Parasitoid females of both species exhibited consistently higher rates of oviposition into their preferred host species and adjusted their reproductive allocation to hosts and host patches as a function of their experience in previous patches.     

Coping with multiple enemies – the evolution of resistance and host-parasitoid community structure

Recent work has shown that the evolution of Drosophila melanogaster resistance to attack by the parasitoid Asobara tabida is constrained by a trade-off with larval competitive ability. However, there are two very important questions that need to be answered. First, is this a general cost, or is it parasitoid specific? Second, does a selected increase in immune response against one parasitoid species result in a correlated change in resistance to other parasitoid species? The answers to both questions will influence the coevolutionary dynamics of these species, and also may have a previously unconsidered, yet important, influence on community structure.     

The response of life‐history traits to a new species in the community: a story of Drosophila parasitoids from the Rhône and Saône valleys

In the present study, we investigated the evolution of life‐history traits in the main species of a community, after the arrival of a new competitor. Two parasitoid species, Leptopilina heterotoma and Asobara tabida, are present throughout the Rhône and Saône valleys, whereas a third species, Leptopilina boulardi, is slowly extending its distribution northwards. In the presence of L. boulardi, competing parasitoids experience a higher mortality and lower host availability. Resources should thus be re‐allocated between traits according to these new factors. We compared life‐history traits of populations of L. heterotoma and A. tabida in areas with and without L. boulardi. As predicted by both Price's balanced mortality hypothesis and the theory of life‐history traits, we found that investment in reproduction is higher in southern populations for both native species, coupled with higher travelling abilities. However, only A. tabida paid their higher fecundity by a lower longevity. The absence of a clear trade‐off between these traits in L. heterotoma may be explained by a lower metabolic rate in southern populations. These results highlight the importance of the community change over climate in the evolution of life‐history traits in this parasitoid community. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.