Influence of a bimodal emergence strategy of a Dipteran host on life-history traits of its main parasitoids

Abstract. 1. Among a great diversity of other strategies, insects have evolved polymodal emergence patterns that can increase survival in the face of annual variations in environmental conditions. Delia radicum L. (Diptera: Anthomyiidae) is a polyvoltine pest that attacks several cultivated cruciferous species. At the time of emergence, most populations show a polymodal emergence of type A (i.e. all individuals that enter diapause in the same year terminate diapause the following growing season, and exhibit a bimodal emergence curve). This results in the occurrence of two sympatric phenotypes, early and late, which differ by the timing of adult emergence in both diapausing and non‐diapausing generations. 2. In Brittany, D. radicum pupae can be heavily parasitised by three parasitoids, Aleochara bilineata Gyll. (Coleoptera: Staphylinidae), Aleochara bipustulata L., and Trybliographa rapae (Hymenoptera: Eucoilidae). As in all parasitoids species, the successful development of both Aleochara species and T. rapae larvae depends mainly on the amount and quality of the food provided by the host. 3. The relationship between early and late host phenotype and (i) the parasitism efficiency, (ii) emergence patterns, and (iii) host selection behaviour were investigated for the three parasitoid species. 4. Depending on parasitoid species and their different parasitism and development mode, the results reveal that host phenotype can influence (i) survival and development time in T. rapae, and (ii) survival in Aleochara species. Aleochara larvae did not appear to discriminate between early and late host pupae on the basis of phenotype, but rather selected them according to their developmental stage. Furthermore, it was discovered that the same phenological strategy occurred in T. rapae and in D. radicum. However, for D. radicum the results indicate that such a strategy has a cost as the longer development time of late host pupae results in a longer period of time favourable for parasitism.     

Effects of conservation strip and crop type on natural enemies of Delia radicum

This 3‐year field study investigated the combined effect of floral resources and perennial shelter habitats (i.e. conservation strips), and crop rotation in supporting natural enemies of the cabbages root fly, Delia radicum. Habitat manipulation with conservation strips increased the overall catches of hymenopteran parasitoids. However, conservation strips did not increase parasitism by either of the two dominant parasitoid species, Trybliographa rapae and Aleochara bipustulata, in any study year. In fact, higher parasitism was found in control plots in the second year. This could be explained by parasitoid mobility and higher patch detectability, as more plants in the control plots were infested with D. radicum larvae. Conservation strips did not result in increased predation of D. radicum eggs. However, the activity densities of two Bembidion species were correlated with egg predation. The species assemblage distribution of epigeal predators was best explained by seasonal period, followed by year and, to a low extent, crop type, while treatment with conservation strips had no effect. However, during the egg laying peak of D. radicum, a higher number of A. bipustulata, an important larval predator was observed in conservation strips during one study year. In conclusion, positive effects of conservation strips were demonstrated for abundance of some natural enemies of D. radicum, but a consistent increase in performance could not be adequately demonstrated due to experimental set‐up, the short timescale and the complex landscape in which our study site was located.     

Dynamic effects of parasitism by an endoparasitoid wasp on the development of two host species: implications for host quality and parasitoid fitness

1. The study reported here examined growth and developmental interactions between the gregarious larval koinobiont endoparasitoid Cotesia glomerata (Hymenoptera: Braconidae) and two of its hosts that vary considerably in growth potential: Pieris rapae and the larger P. brassicae (Lepidoptera: Pieridae). At pupation, healthy larvae of P. brassicae are over twice as large, in terms of fresh body mass, as those of P. rapae. 2. Clutch size of C. glomerata was manipulated artificially, and the relationship between parasitoid burden and the maximum weight of the parasitised host (= host–parasitoid complex) was measured. In both hosts, the maximum complex weight was correlated positively with parasitoid burden. Compared with unparasitised hosts, however, the growth of P. rapae was increased at significantly lower parasitoid burdens than in P. brassicae. Emerging wasp size was correlated negatively with parasitoid burden in both host species, whereas development time was less affected. 3. After larval parasitoid egress, the weight of the host carcass increased slightly, but not significantly, with parasitoid burden, although there was a strong correlation between the proportion of host mass consumed by C. glomerata larvae during development and parasitoid burden. 4. Clutch size was generally correlated positively with instar parasitised in both hosts, and greater in P. brassicae than in P. rapae. Sex ratios were much more female biased in L1 and L2 P. rapae than in all other host classes. Adult parasitoid size was correlated inversely with host instar at parasitism, and wasps emerging from P. brassicae were larger, and completed development faster, than conspecifics emerging from P. rapae. 5. The data reveal that parasitism by C. glomerata has profound species‐specific effects on the growth of both host species. Consequently, optimality models in which host quality is often based on host size at parasitism or unparasitised growth potential may have little utility in describing the development of gregarious koinobiont endoparasitoids. The results of this investigation are discussed in relation to the potential effectiveness of gregarious koinobionts in biological control programmes.     

Spatial ecology of host–parasitoid interactions: a threatened butterfly and its specialised parasitoid

Habitat conservation for threatened temperate insect species is often guided by one of two paradigms: a metapopulation approach focusing on patch area, isolation and number; or a habitat approach focusing on maintaining high quality habitat for the focal species. Recent research has identified the additive and interacting importance of both approaches for maintaining populations of threatened butterflies. For specialised host-parasitoid interactions, understanding the consequences of habitat characteristics for the interacting species is important, because (1) specialised parasitoids are particularly vulnerable to the consequences of fragmentation, and (2) altered interaction frequencies resulting from changes to habitat management or the spatial configuration of habitat are likely to have consequences for host dynamics. The spatial ecology of Cotesia bignellii, a specialist parasitoid of the threatened butterfly Euphydryas aurinia, was investigated at two spatial scales: within habitat patches (at the scale of individual aggregations of larvae, or ‘webs’) and among habitat patches (the scale of local populations). Parasitism rates were investigated in relation to larval web size, vegetation sward height and host density. Within patches, the probability of a larval webs being parasitized increased significantly with increasing number of larvae in the web, and parasitism rates increased significantly with increasing web isolation. The proportion of webs parasitized was significantly and negatively correlated with cluster density. Among habitat patches the proportion of parasitized webs decreased as cluster density increased. Clusters with a high proportion of larval webs parasitized tended to have lower parasitism rates per larval web. These results support the call for relatively large and continuous habitat patches to maintain stable parasitoid and host populations. Conservation efforts directed towards maintenance of high host plant density could allow E. aurinia to reduce parasitism risk, while providing C. bignellii with sufficient larval webs to allow population persistence.     

Aboveground herbivory affects indirect defences of brassicaceous plants against the root feeder Delia radicum Linnaeus: laboratory and field evidence

1. Belowground herbivory has recently been shown to disrupt the host location behaviour of aboveground parasitoids and thereby impact plants indirect defences. Reverse interactions, on the other hand, have received little attention so far. 2. Lab and field studies were conducted to examine whether the presence of the leaf herbivore Pieris brassicae Linnaeus on brassicaceous plants influences the response of Trybliographa rapae Westwood, a specialist parasitoid of the root feeder Delia radicum Linnaeus. 3. The present results show that the attraction of the parasitoid towards host‐infested plants disappeared when these plants were also infested by P. brassicae. This absence of attraction was observed both when the complete odour blend or only undamaged leaves from damaged plants were offered, emphasising the role of systemically induced volatiles for host location in T. rapae. 4. Furthermore, the field study revealed that parasitism levels dropped from 30% on root‐infested plants to 4% on double‐infested plants. 5. The present study is the first to confirm that reduced attraction to host‐infested plants as a result of simultaneous attack by below‐ and aboveground herbivores translates into lower levels of parasitism in the field.     

Insect-crop interactions in a diversified cropping system: parasitism by Aleochara bilineata and Trybliographa rapae of the cabbage root fly, Delia radicum, on cabbage in the presence of white clover

Parasitism of the cabbage root fly, Delia radicum (L.) by the staphylinid Aleochara bilineata Gyllenhal and the cynipid Trybliographa rapae Westwood was examined in a cabbage monoculture and a mixed stand of cabbage undersown with white clover. Number of overwintering cabbage root fly pupae per plant was consistently reduced in the mixed stand, and the incidence of plants attacked by cabbage root fly was either reduced or not different in the mixed stand compared to cabbage monoculture. For both parasitoids, the probability of D. radicum attacked plants having at least one parasitized pupa increased with density of cabbage root fly pupae around the plant. For A. bilineata, this positive relation between presence of parasitism and host density was consistently stronger in cabbage monoculture than in cabbage undersown with clover. Location of a host plant by T. rapae was not consistently affected by the presence of clover. D. radicum attacked plants situated in the cabbage and clover mixture were found by T. rapae as easily as in cabbage monoculture. Overall, the total risk of parasitism for a cabbage root fly pupa by A. bilineata was reduced in the mixed stand compared to the cabbage monoculture, whereas the risk of parasitism by T. rapae was not consistently affected by clover. For both parasitoids, intensity of parasitism showed a variable relationship with host density on individual plants attacked by the cabbage root fly. Overall, in spite of consistently lower total density of pupae in the mixed cabbage—clover than in cabbage monoculture, the density of unparasitized pupae was reduced by the presence of non-host plants only in two of the four experiments. The results emphasize the need to include not only herbivore and crop, but also other plant species as well as natural enemies when evaluating management methods.     

Seasonal phenology and stage-specific parasitism of the apple ermine moth, Yponomeuta malinellus Zeller, in Korea

The apple ermine moth, Yponomeuta malinellus Zeller (Lepidoptera: Yponomeutidae), is a tent caterpillar that feeds on Malus spp. in Korea. Populations of the moth in native areas appeared to be regulated by the assemblage of parasitoids. Phenological associations between host stages and parasitoids, susceptible stage(s) of the host for each parasitoid, and stage‐specific parasitism were studied. The egg larval parasitoid Ageniaspis fuscicollis (Dalman) had highest parasitism of first instar larvae (24%), with 14% parasitism of other larval stages. Dolichogenidea delecta (Haliday) was recovered from all larval instars with the highest parasitism rate of second instar larvae (20.1%), followed by 19.9% parasitism of mid‐larval hosts. Herpestomus brunicornis Gravenhorst was reared from second instar larvae through to pupal collection, and had the highest parasitism rate (29.9%) at the pupal stage. The larval pupal parasitoid Zenillia dolosa (Meigen) was recovered from mid‐larval to pupal stages with the highest parasitism rate (5.5%) occurring in third to fourth instar larvae. The host stages for developing A. fuscicollis completely overlap with those of D. delecta, and with those of H. brunicornis to some degree. A statistically significant negative correlation exists between A. fuscicollis and these dominant parasitoids, indicating competitive interaction within the host.     

Patterns of parasitism by Trybliographa rapae, a cynipid parasitoid of the cabbage root fly, under laboratory and field conditions

ABSTRACT.

• 1 The spatial patterns of parasitism of the cabbage root fly caused by the cynipid parasitoid Trybliographa rapae (Westw.) have been studied in a laboratory system, within field cages and in a natural situation.
• 2 Continuous observations during the laboratory experiments showed the parasitoids to spend proportionately more time on the patches of high host density. This resulted in the per cent parasitism per patch being directly density dependent.
• 3 Similar patterns of parasitism were found from the field cage system, and also from experiments using the natural parasitoid population and either manipulated or natural host densities.
• 4 While mutual interference was marked in the laboratory experiments, there was little or no sign of it within the larger field cages.

     

Parasitoid–Pathogen–Pest Interactions of Chelonus insularis, Campoletis sonorensis, and a Nucleopolyhedrovirus in Spodoptera frugiperda Larvae

In this study we examined interactions between two solitary endoparasitoids, the braconid Chelonus insularis and the ichneumonid Campoletis sonorensis, and a multiple-enveloped nucleopolyhedrovirus infecting Spodoptera frugiperda larvae. We examined whether ovipositing females minimize interference by discriminating amongst hosts and examined the outcome of within-host competition between parasitoid species and between the parasitoids and the virus. The egg–larval parasitoid Ch. insularis did not discriminate between virus-contaminated and uncontaminated S. frugiperda eggs; all S. frugiperda larvae that emerged from surface-contaminated eggs died of viral infection prior to parasitoid emergence. The larval parasitoid C. sonorensis also failed to discriminate between healthy and virus-infected S. frugiperda larvae or between larvae unparasitized or parasitized by Ch. insularis. Host larvae parasitized in the egg stage by Ch. insularis were suitable for the development of C. sonorensis when they were multiparasitized by C. sonorensis as first, second, third, and fourth instars, whereas emergence of Ch. insularis was dramatically reduced (by 85 to 100%) in multiparasitized hosts. Nonspecific host mortality was significantly higher in multiparasitized hosts than in singly parasitized hosts. The development time and sex ratio of C. sonorensis in multiparasitized host larvae were unaffected by the presence of Ch. insularis larval stages. Both Ch. insularis parasitized and nonparasitized larvae of the same instar (second, third, or fourth instars) had a similar quantitative response to a challenge of virus inoculum. All host larvae that ingested a lethal dose of virus were unsuitable for Ch. insularis development. In contrast, C. sonorensis did not survive in hosts that ingested a lethal virus dose immediately after parasitism, but parasitoid survival was possible with a 2-day delay between parasitism and viral infection and the percentage of parasitoid emergence increased significantly as the interval between parasitism and viral infection increased. The development time of C. sonorensis was significantly reduced in virus-infected hosts compared to conspecifics that developed in healthy hosts. C. sonorensis females that oviposited in virus-infected hosts did not transmit the virus to healthy hosts that were parasitized subsequently. Field applications of virus for biocontrol of S. frugiperda may lead to substantial mortality of immature parasitoids, although field experiments have not yet demonstrated such an effect.     

Parasitism by Pteromalus cerealellae (Hymenoptera: Pteromalidae) on the Cowpea weevil, Callosbruchus maculatus (Coleoptera: Bruchidae): Host density, temperature effects, and host finding ability

Studies on interactions between a larval parasitoid, Pteromalus cerealellae (Boucek) and one of its hosts, Callosobruchus maculatus (F.) were carried out in the laboratory. The number of host larvae parasitized by P. cerealellae increased with host larvae at low densities and tended to a plateau at a density of 25 larvae per female parasitoid. Each parasitoid was able to parasitize more hosts and produced more offspring at 20 and 25 °C than at 30 °C. The number of non-infested seeds mixed with seeds infested with the last instar of C. maculatus did not preclude P. cerealellae from identifying infested seeds and attacking larvae inside them. When infested seeds were tightly packed, several host larvae escaped parasitism. P. cerealellae may be a useful biological control agent in newly harvested cowpea with low C. maculatus infestation, and lowering the temperature of the storage system may enhance the effectiveness of this parasitoid.     

Varying degree of physiological integration among host instars and their endoparasitoid affects stress‐induced mortality

In natural populations of insect herbivores, genetic differentiation is likely to occur due to variation in host plant utilization and selection by the local community of organisms with which they interact. In parasitoids, engaging in intimate associations with their host during immature development, local variation may exist in host quality for parasitoid development. We compared the development of a gregarious endoparasitoid, Cotesia glomerata L. (Hymenoptera: Braconidae), collected in The Netherlands, in three strains and three caterpillar instars (L1–L3) of its main host, Pieris brassicae L. (Lepidoptera: Pieridae). Hosts had been collected in The Netherlands and France, and were reared in the laboratory for one generation. We also used an established Dutch laboratory strain that had not been exposed to parasitoids for at least 24 generations. Parasitoid survival to adulthood was inversely correlated with host instar at parasitism. Adult parasitoid body mass was largest when hosts were parasitized as L1 and smallest when hosts were parasitized as L3, whereas egg‐to‐adult development time was quickest on L3 hosts and slowest on L1 hosts. Higher survival and faster development of C. glomerata on French L2 hosts also showed that there is variation in host‐instar‐related suitability. Many L2 and most L3 caterpillars that were parasitized exhibited signs of pathogen infection and perished within a few days of parasitism, whereas this never happened when hosts were parasitized as L1 or in non‐parasitized control caterpillars. Our results reveal that, irrespective of the host strain, L1 hosts are optimally synchronized with C. glomerata development. By contrast, the high precocious mortality of L3 larvae may be due to stress‐induced regulation by the parasitoid in order to ‘force’ its developmental program into synchrony with the developing parasitoid larvae. Our results underscore a potentially important role played by pathogens in mediating herbivore–parasitoid interactions that are host‐instar‐dependent in their expression.     

Growth and development of Cardiochiles nigriceps viereck (hymenoptera,braconidae) larvae and their synchronization with some changes of the hemolymph composition of their host,Heliothis virescens (F.) (Lepidoptera,Noctuidae)

Larval development of the parasitoid Cardiochiles nigriceps Viereck occurs in the last instar larva of its host, Heliothis virescens (F.). This allows the parasitoid to exploit the nutritional increase in the biosynthetic activity occurring in the host in preparation for metamorphosis. To understand the biochemical basis of this host parasitoid developmental synchrony, we undertook host ligation studies and analyzed host hemolymph for proteins and glycerol esters. Parasitization affected the biochemical profile of the host. The hemolymph protein concentration of parasitized last instar H. virescens larvae increased through time, whereas unparasitized (control) larvae were characterized by a decrease in the protein titer when they reached the prepupal stage. The effect of parasitism on glyceride titers of host hemolymph was not as pronounced as the effect on proteins. Ligation conducted on 5th instar hosts, which were parasitized as 4th instars, affected parasitoid development in a time-dependent way. The percentage of successfully developing C. nigriceps larvae increased with the increase of the time interval between parasitization and ligation. Ligation performed before day 2 of the 5th larval instar of H. virescens completely inhibited parasitoid development. Ligations that disrupted parasitoid developmentwere associated with a low host hernolymph protein concentration. Parasitoid development was successful when hernolymph protein titer was high, as occurred when ligations were performed after day 3 of the 5th host instar in both control and parasitized larvae. Ligations in both situations resulted in a slight increase in glyceride titers. The results suggest that host proteins and/or some factor(s) associated with them may play a role in parasitoid growth and development. © 1993 Wiley-Liss, Inc.     

Effect of food plant switching by a herbivore on its parasitoid: Cotesia melanoscela development in Lymantria dispar exposed to reciprocal dietary crosses

1. Host plant switching by dispersing early instar lepidopterans could have implications for parasitoid performance, but this possibility has not been evaluated thoroughly. 2. The relative growth rates of Lymantria dispar parasitized by Cotesia melanoscela, and the weight of larvae at the time of parasitoid emergence, were affected most by the second larval food plant consumed. 3. The relative growth rates, pupal weights, weight of larva at the time of parasitoid emergence, and development times of L. dispar were affected significantly by the second larval food plant consumed. 4. Development time and size of Cotesia melanoscela were affected most by the second larval food plant consumed. 5. Parasitoid performance was affected most by the larval host’s relative growth rate and the final weight of the host larva at the time of parasitoid emergence. 6. Host plant switching affected the weight of L. dispar larvae at the time of parasitoid emergence, but the effect of switching per se was not a significant factor in C. melanoscela size or development. 7. Lymantria dispar larvae that fed on Populus as their second host outperformed larvae that fed ultimately on Acer. 8. Parasitoids yielded from L. dispar larvae that fed ultimately on Populus outperformed parasitoids yielded from larvae that fed ultimately on Acer. 9. Per cent mortality of L. dispar due to parasitism and percentage adult C. melanoscela emergence were highest in parasitized larvae fed Populus, poor in hosts fed Acer, and intermediate in switching larvae.     

Fecundity and Longevity of Green Vegetable Bug,Nezara viridula, Following Parasitism byTrichopoda giacomellii

The effects of parasitism by the ArgentinianTrichopoda giacomellii(Blanchard) on reproduction and longevity of its host,Nezara viridula(L.) are reported. Parasitoid larvae suppress egg maturation, reducing by 70% the fecundity of mature female hosts during the period of larval development. Egg viability was not affected, but mating frequency was reduced by approximately 50%. When parasitized as newly eclosed adults, 84% of females fail to reproduce. In male hosts, fertility and mating frequency were not affected during the period of larval parasitoid development. In male and reproductively immature female hosts, death was coincident with, or occurred shortly after parasitoid emergence (2–4 days); in mature females, death occurred on average 2 weeks after larval parasitoid emergence. Host mortality occurred as a consequence of tissue damage incurred as the parasitoid larvae emerged from the host. Some individuals survived parasitism though no further reproductive activity (mating or oviposition) occurred. The effectiveness ofT. giacomelliias a biological control agent is discussed in relation to its impact on reproduction and survival of its host and contrasted with the action of otherTrichopodaspecies.     

Dose-dependent influence of Microplitis rufiventris factors on developmental rate and growth of last-instar Spodoptera littoralis larvae

The solitary endoparasitoid, Microplitis rufiventris, attacks and can develop in earlier instars of Spodoptera littoralis larvae with preference to third‐instar larvae. We used the last stadium (sixth instar), a stage which is not naturally parasitized. The newly moulted larvae (0–3 h old) of this stadium were more acceptable for parasitization by the wasp females than the older ones (24 h old). Parasitization by M. rufiventris wasp of last instar S. littoralis larvae leads to dose (no. of eggs + parasitoid factors)‐dependent effects which were more pronounced at 20°C than at 27°C. A single oviposition into a sixth instar host larva resulted in normal development of the host. However, superparasitization increased the proportions of developmentally arrested hosts and number of live wasp larvae. Development of supernumerary individuals of the parasitoid in the host larva leads to dose‐related adverse effects on host growth and development. The present study may provide interesting opportunities for studying the physiological bases of host–parasitoid interactions and parasitoid intra‐specific competition in the biological system considered.     

Spatio-temporal distribution patterns of two tachinid flies,Epicampocera succincta andCompsilura concinnata parasitizingPieris

Larvae of genus Pieris in the northern part of Kyoto City are parasitized by two tachinid flies:Epicampocera succincta, a specialist on genus Pieris, and Compsilura concinnata, a generalist with very wide host-range. We surveyed the parasitism rates of Pieris by both flies for two years at six study areas. In these study areas, there lived three host species in the genus Pieris: P. rapae, P. melete, and P. napi, but neither tachinid parasitized P. napi to any significant extent. In the mountainous district, P. rapae and P. melete coexisted and their populations were relatively continuous, while in the lowland, only P. rapae larvae were abundant in spring and autumn, but even they disappeared in summer. Parasitisms by E. succincta occurred mainly in mountainous district and never in the lowland. C. concinnata parasitized Pieris in all the areas, but its parasitisms occurred mainly in autumn. We analyzed the factors affecting the spatial and temporal patterns of parasitism rates and presumed that the temporal discontinuity of host population restricted the distribution of the specialist parasitoid.     

Response of the wasp (<Emphasis Type="Italic">Cotesia glomerata</Emphasis>) to larvae of the large white butterfly (<Emphasis Type="Italic">Pieris brassicae</Emphasis>)

The large white butterfly (Pieris brassicae L) first invaded northernmost Japan from Siberia around 1994, and after a few years, began to expand its range. The wasp, Cotesia glomerata (L) parasitizes larvae of the small white butterfly (Pieris rapae crucivora Boisduval), a usual host in the same geographic area. Some Pieris brassicae larvae in Hokkaido have been parasitized by Cotesia glomerata, but the parasitism rate of Pieris brassicae larvae tends to be lower than that of Pieris rapae. To examine the process of parasitizing Pieris brassicae larvae, we observed how the parasitoid wasp responded to the host larvae on damaged leaves. Cotesia glomerata females tended to avoid Pieris brassicae larvae, and even when female wasps inserted their ovipositors into Pieris brassicae larvae, none laid eggs. The parasitoids obtained from Pieris rapae larvae failed to parasitize Pieris brassicae during the host-acceptance step.     

Performance of Microplitis tuberculifer (Hymenoptera: Braconidae) parasitizing Mythimna separata (Lepidoptera: Noctuidae) in different larval instars

The solitary parasitoid Microplitis tuberculifer (Wesmael) is an important biological control agent of various lepidopteran pests in Asia. We examined the preference of M. tuberculifer for different instars of its common host, Mythimna separata (Walker), host instar effects on parasitoid development, and the consequences of parasitism in different stages for growth and consumption of host larvae. The wasp successfully parasitized the first four larval instars of M. separata, but not the fifth, which appeared to be behaviorally resistant. First and second instars were parasitized at higher rates compared to thirds and fourths in no-choice situations, ostensibly due to longer handling times for the latter, but second instars were most preferred in a choice test that presented all stages simultaneously. Although later instar hosts yielded heavier cocoons, the fastest parasitoid development was obtained in second instars. Lower sex ratios were obtained from first instars as females appeared to lay a smaller proportion of fertilized eggs in small hosts. Both weight gain and food consumption of parasitized larvae were reduced significantly within 24 h of parasitism, regardless of the stage parasitized, and final body weights were less than 10% those of unparasitized larvae. Thus, M. tuberculifer has good potential as a biological control agent of M. separata, successfully parasitizing the first four larval instars and dramatically reducing plant consumption by the host in all cases.     

Spatial aggregation across ephemeral resource patches in insect communities: an adaptive response to natural enemies?

Although an increase in competition is a common cost associated with intraspecific crowding, spatial aggregation across food-limited resource patches is a widespread phenomenon in many insect communities. Because intraspecific aggregation of competing insect larvae across, e.g. fruits, dung, mushrooms etc., is an important means by which many species can coexist (aggregation model of species coexistence), there is a strong need to explore the mechanisms that contribute to the maintenance of this kind of spatial resource exploitation. In the present study, by using Drosophila-parasitoid interactions as a model system, we tested the hypothesis whether intraspecific aggregation reflects an adaptive response to natural enemies. Most of the studies that have hitherto been carried out on Drosophila-parasitoid interactions used an almost two-dimensional artificial host environment, where host larvae could not escape from parasitoid attacks, and have demonstrated positive density-dependent parasitism risk. To test whether these studies captured the essence of such interactions, we used natural breeding substrates (decaying fruits). In a first step, we analysed the parasitism risk of Drosophila larvae on a three-dimensional substrate in natural fly communities in the field, and found that the risk of parasitism decreased with increasing host larval density (inverse density dependence). In a second step, we analysed the parasitism risk of Drosophila subobscura larvae on three breeding substrate types exposed to the larval parasitoids Asobara tabida and Leptopilina heterotoma. We found direct density-dependent parasitism on decaying sloes, inverse density dependence on plums, and a hump-shaped relationship between fly larval density and parasitism risk on crab apples. On crab apples and plums, fly larvae benefited from a density-dependent refuge against the parasitoids. While the proportion of larvae feeding within the fruit tissues increased with larval density, larvae within the fruit tissues were increasingly less likely to become victims of parasitoids than those exposed at the fruit surface. This suggests a facilitating effect of group-feeding larvae on reaching the spatial refuge. We conclude that spatial aggregation in Drosophila communities can at least in part be explained as a predator avoidance strategy, whereby natural enemies act as selective agents maintaining spatial patterns of resource utilisation in their host communities.