Avoidance mechanisms of three Pieris butterfly species against the parasitoid wasp Apanteles glomerulus

Abstract. 1. Experimental studies have shown that larvae of three Pieris butterflies, P.rapae L., P.melete Mènètriés and P.napi L., are attacked by a parasitoid wasp, Apanteles glomeratus L. Although P.rapae larvae are parasitized heavily in the field, P.melete and P.napi are infrequently parasitized successfully because they possess mechanisms for encapsulating parasitoid larvae and for avoiding parasitism.
2. This study examines spatial and temporal variation in rates of parasitism of the three Pieris species by A.glomeratus in the field. We attempted to determine whether P.rapae possesses any means of avoiding parasitism by this wasp, and then to deduce why both P.melete and P.napi have more distinctive avoidance mechanisms than P.rapae.
3. Our results indicate that in temporary habitats, which are the main habitats of P.rapae, P.rapae is able to escape A.glomeratus in time and space by colonizing new habitats before the parasitoid arrives. In permanent habitats, however, such escape is not possible. P.rapae larvae lack physiological or behavioural avoidance mechanisms of reducing parasitism rates in permanent habitats. P.melete and P.napi , in contrast, live only in permanent habitats, where the parasitic pressure is potentially high, and have evolved active avoidance mechanisms.     

Factors affecting host selection in an insect host–parasitoid interaction

1. Many parasitoids can develop successfully in different stages of the same host but the costs of parasitism may vary between the stages. The stage of host attacked has generally been determined when there is no choice, giving a misleading impression of host selection or preference.
2. The rate of parasitism by a solitary endoparasitoid, Venturia canescens , of each larval stage of the Indian meal moth, Plodia interpunctella , was examined with and without a host refuge from parasitism. In addition, when given a choice of host stages, with and without a refuge, the influence of parasitoid age on host selection was examined.
3. Wasps were able to parasitize all except the first instar, but second instars experienced significantly reduced parasitism, in both refuge treatments, compared with third to fifth instars. Whilst parasitoid emergence was always significantly less when all host stages had a refuge, the reduction was only marginally significant when second instars were attacked.
4. When given a choice of second- and fifth-instar larvae, wasps consistently parasitized more fifth instars, both with and without a refuge. Moreover, significantly fewer second-instar larvae were parasitized in the presence of fifth instars than when presented alone to the wasps. This pattern of parasitism was unaffected by the increasing age of the parasitoids.
5. Host selection by V. canescens is discussed in terms of host–parasitoid population dynamics and structure.     

Influences of host feeding-niche and foodplant type on generalist and specialist parasitoids

Abstract. 1. We classified the parasitoids of 185 British herbivorous insect species as being koinobionts (which should tend to be specialists) or idiobionts (potential generalists) to examine the influences of host feeding-niche and foodplant type on the numbers of parasitoid species attacking individual host species.
2. The majority of parasitoid species of exophytic hosts are koinobionts, whereas endophytic hosts support mainly idiobionts.
3. Parasitoid assemblage size increases with host foodplant size and complexity; for endophytic hosts this is due to an increase in idiobionts on hosts on large plants, but for exophytic hosts it is the number of koinobionts that increases with foodplant size.
4. Comparison of these patterns with those predicted under a competition hypothesis suggests that parasitoid communities associated with endophytic hosts may be commonly limited by interspecific competition, whereas those of exophytic hosts probably are not.     

Bottom-up cascading effects in a tritrophic system: interactions between plant quality and host-parasitoid immune responses

Abstract.  1. Little is known about underlying mechanisms by which plants indirectly affect parasitism success in hymenopteran endoparasitoids. The hypothesis that host-plant effects can challenge the innate immune system of an insect host was experimentally tested in this study using a model tritrophic, crucifer – lepidopteran [ Plutella xylostella (L.)] – parasitoid [ Cotesia plutellae (Kurdjumov)], system.
2. The effects of host-plant suitability on herbivore performance and parasitism were examined. The bottom-up effect of plant suitability on host-parasitoid immune responses was then evaluated using measures of cellular and humoral effectors.
3. Host-plant quality showed a significant effect on the encapsulation response of P. xylostella to first instar but not to second instar parasitoid larvae. Encapsulation was never sufficient to prevent parasitoid emergence.
4. Poor host-plant suitability suppressed phenoloxidase activity in the absence of the parasitoid. The suppressive effect of C. plutellae on phenoloxidase activity was much greater and no plant effects were detectable after insects had been parasitized.
5. Despite strong plant effects on parasitism, those on immune effectors of the host were transitory or overwhelmed by the effect of the parasitoid.
6. These results demonstrated that plant-mediated variation in parasitism success by C. plutellae were not as a result of plant nutritional status or other attributes affecting the immune function of P. xylostella , nor to host-plant effects on superparasitism.
7. In these experiments, P. xylostella was a fully permissive host to C. plutellae and host-plant-mediated effects on the innate immune response appeared to play no part in parasitoid survival within hosts.     

Differences in host plant selection among three Athalia sawflies feeding on crucifers in Japan

Abstract 1. The ways of using host plants were compared among the three Athalia sawflies [ A. japonica (Klug), A. rosae ruficornis Jakovlev, and A. infumata (Marlatt)] feeding on crucifers in Japan to determine whether host specialisation can explain the difference in their life-history traits. The occurrence of their larvae was examined on each crucifer species in the field, and the suitability of each crucifer species for the three successive steps of host use by the sawflies was evaluated: microhabitat selection by adult females, female oviposition, and larval growth.
2. There were 11 species of crucifer in the study area, and A. japonica , A. rosae , and A. infumata used nine, seven, and eight species respectively. Thus, sawfly host ranges overlapped.
3. Adult females of A. japonica , A. rosae , and A. infumata preferred shady clumps of crucifers, sunny clumps of crucifers, and disturbed areas respectively.
4. Unsuitable hosts for larval performance such as Brassica oleracea and Arabis plants were eliminated from the host ranges of the three sawflies.
5. Once they chose microhabitats, the suitability of each host plant for female oviposition and larval growth was similar.
6. Because of the divergent preferences for microhabitats, the host plants that were suitable for all the three steps were restricted to different sets of plants among the sawflies: Cardamine for A. japonica , cultivated crucifers ( Raphanus and Brassica ) for A. rosae , and Rorippa for A. infumata . These plants could be recognised as the respective primary host plants.
7. The spatio-temporal distributions of primary hosts were consistent with and explained the pattern of diapause and migration of each sawfly, suggesting that host specialisation caused their life-history traits to differentiate.     

Contrary choices: possible exploitation of enemy-free space by herbivorous insects in cultivated vs. wild crucifers

Summary The pressure to escape natural enemies may shape how herbivorous insects use their plant resources. On wild crucifers, ovipositional preferences of the diamondback moth (Plutella xylostella; DBM) were similar to searching preferences of its main parasitoid, an ichneumonid wasp (Diadegma insulare). But on cultivated crucifers, these species had opposite preferences. In addition, DBM ovipositional preferences did not correlate with growth or reproduction on several foodplants. We interpret these patterns as evidence of evolution for use of enemy-free space in agricultural systems.     

Consequences for a host–parasitoid interaction of host-plant aggregation, isolation, and phenology

Abstract.  1. Spatial habitat structure can influence the likelihood of patch colonisation by dispersing individuals, and this likelihood may differ according to trophic position, potentially leading to a refuge from parasitism for hosts.
2. Whether habitat patch size, isolation, and host-plant heterogeneity differentially affected host and parasitoid abundance, and parasitism rates was tested using a tri-trophic thistle–herbivore–parasitoid system.
3.  Cirsium palustre thistles ( n = 240) were transplanted in 24 blocks replicated in two sites, creating a range of habitat patch sizes at increasing distance from a pre-existing source population. Plant architecture and phenological stage were measured for each plant and the numbers of the herbivore Tephritis conura and parasitoid Pteromalus elevatus recorded.
4. Mean herbivore numbers per plant increased with host-plant density per patch, but parasitoid numbers and parasitism rates were unaffected. Patch distance from the source population did not influence insect abundance or parasitism rates. Parasitoid abundance was positively correlated with host insect number, and parasitism rates were negatively density dependent. Host-plant phenological stage was positively correlated with herbivore and parasitoid abundance, and parasitism rates at both patch and host-plant scales.
5. The differential response between herbivore and parasitoid to host-plant density did not lead to a spatial refuge but may have contributed to the observed parasitism rates being negatively density dependent. Heterogeneity in patch quality, mediated by variation in host-plant phenology, was more important than spatial habitat structure for both the herbivore and parasitoid populations, and for parasitism rates.     

Low parasitoid success on a myrmecophilous host is maintained in the absence of ants

Abstract.  1. Studies of Dinocampus coccinellae , a parasitoid of ladybird beetles, have generally shown congruence between field parasitism rates of different host species and parasitoid preference and/or host suitability in the laboratory, suggesting that host intrinsic factors rather than habitat-related extrinsic factors are of greatest importance in determining D. coccinellae occurrence.
2. The myrmecophilous Coccinella magnifica exhibits much lower D. coccinellae prevalence in the field than most other Coccinella species: it has been suggested that this is a manifestation of enemy-free space provided by the predatory Formica rufa group ants with which the C. magnifica occurs.
3. Coccinella magnifica collected at the same time and locality as parasitised Coccinella septempunctata were unparasitised by D. coccinellae . In the laboratory, in the absence of ants, although the parasitoid attacked C. magnifica as readily as C. septempunctata , C. magnifica was not parasitised successfully.
4. Such results are consistent with those from other ladybirds and C. magnifica does not now benefit directly from any putative D. coccinellae -free space provided by aggressive ants. Because its close relatives exhibit high levels of D. coccinellae parasitism, C. magnifica may be useful in determining some elements important in the evolution of host protection against parasitoid attack.     

Effect of Sequential Learning Experiences on Searching Responses and Sex Ratio Allocations of the Gregarious Insect Parasitoid, Cotesia congregata (Say) (Hymenoptera: Braconidae)

We investigated the effects of sequential adult learning experiences (postemergence + ovipositional) with two host foodplants (tomato and/or tobacco) on searching responses, clutch size, and sex ratio allocations of Cotesia congregata, a gregarious endoparasitoid of Manduca sexta. Sequential experiences with one host foodplant resulted in a stronger searching response to the plant experienced and a higher proportionate allocation of females to hosts offered with this plant. Sequential experiences with both plants resulted in similar searching responses to the two plants and similar proportionate allocations of females, irrespective of the order in which plants were experienced. Ovipositional experience resulted in a stronger searching response to the plant experienced but effects on sex ratio allocations were not definitive. Clutch size was not modified by experience. Results demonstrate that parasitic wasps can learn multiple host-associated plant cues and suggest that sequential learning experiences serve to define the effective host foodplant range.     

Effects of selected insecticides on Diadegma semiclausum（Hymenoptera： Ichneumonidae） and Oomyzus sokolowskii （Hymenoptera： Eulophidae）, parasitoids of Plutella xylostella （Lepidoptera： Plutellidae）

Abstract Field doses of six selected insecticides were tested against the immature (pupae) and mature (adult) stages of Diadegma semiclausum (Hellén) and Oomyzus sokolowskii (Kurdjumov), parasitoids of the diamondback moth, Plutella xylostella (L.). Effects of contact toxicity (direct spraying) of the six insecticides on emergence of parasitoids were found negligible on both species except permethrin which caused 37.5% mortality. All adults of both parasitoid species died 24 hours after exposure to chlorfenapyr, emamectin benzoate and permethrin. In contrast, the three insect growth regulators (IGRs), chlorfluazuron, flufenoxuron and teflubenzuron, were found harmless to both species, and adult mortality of both parasitoid species was 0–16.7%. However, parasitism by the females of both parasitoid species was severely impaired when the females were offered the three IGR diluted solutions for 24 hours. Effects of oral toxicities of the IGRs on longevity of both parasitoids after 12 hours exposure were found to be significantly different between males and females. Compatibility of tested insecticides with D. semiclausum and O. sokolowskii and integration of compatible insecticides with these parasitoids in integrated pest management programs of crucifers are discussed.     

Behaviour of a specialist parasitoid, Cotesia melitaearum: from individual behaviour to metapopulation processes

Abstract. 1. Foraging behaviour and movement within and among host patches of the specialist parasitoid wasp Cotesia melitaearum (Braconidae) attacking the larvae of Melitaea cinxia (Nymphalidae) were studied in the field and in the laboratory.
2. In the field, female wasps aggregated in large host groups in the autumn and caused positive spatial density-dependent parasitism in the field. Wasps stayed longer with groups of pre-diapause caterpillars than with post-diapause caterpillars, but attacked them less frequently.
3. In the laboratory, wasps attacked larger larvae more readily than smaller larvae. Also in the laboratory, wasps exposed to larvae outside their protective webs showed differences in the rates at which they attacked larvae fed different diets, implicating host plant-derived chemicals as proximate cues for foraging wasps.
4. Mark–recapture studies indicated that there was a low rate of successful movement of wasps among groups of young larvae within a habitat patch in the autumn and no successful movement of wasps across non-habitat. In contrast, wasps moved frequently among groups of late-instar caterpillars in the spring.
5. Host caterpillars of different ages responded very differently to wasp attacks. Pre-diapause larvae remained in groups and used collective head-jerking behaviour to defend themselves, whereas post-diapause larvae dispersed away from the group immediately after being attacked.
6. Population and metapopulation level dynamics of the host–parasitoid interaction are discussed in light of these observations of the behaviour of individual wasps.     

Movement of an insect parasitoid in simple and diverse plant assemblages

Abstract. 1. It has been proposed that herbivore populations are lower in diverse than in simple plant habitats because of greater abundance and/or higher efficiency of natural enemies in mixed plant stands. However, higher enemy colonization is expected in monorather than multispecific vegetation if the response of specialist natural enemies to habitat diversification is similar to that of monophagous herbivores.
2. We used release-recapture experiments to determine how the presence of maize (non-host plant) influences the movement of the parasitoid Pediobius foveolatus in the absence of hosts. We then assessed how vegetation diversity affects wasp reproduction (parasitism) and subsequent density in the presence of its hosts, Mexican bean beetle larvae.
3. Fewer female wasps immigrated into and more emigrated out of a bean-tall maize intercrop than bean monocultures. Bean plant density and the presence of maize per se did not significantly affect parasitoid immigration. Instead, maize height was the primary factor contributing to lower female immigration into the bean-tall maize plots. However, tall maize plants did not impede the wasps' within-habitat movement.
4. When wasps were released outside the plots, higher parasitism was recorded in monocultures, irrespective of host density. In contrast, when wasps were released within the plots, significantly higher parasitism rates were found in the bean-tall maize habitat.
5. Results suggest that female wasps accumulate in the bean-tall maize habitat in response to resources other than hosts and, ultimately, wasp density may be determined primarily by differential emigration rather than by immigration rates.     

The reproductive strategy of the gregarious parasitoid,Pteromalus puparum (Hymenoptera: Pteromalidae)

Summary Pteromalus puparum is a gregarious parasitoid of lepidopterous pupae. To determine in which phase of a host outbreak superparasitism occurs, field investigations were carried out on seasonal prevalence of the host, Papilio xuhtus, and parasitism by P. puparum in a citrus grove in Fukuoka, Japan in 1974. Host pupation occurred from May to November and the parasitoid attacked the host throughout this period. Pupal density increased rapidly after mid-August and the percentage parasitism decreased during this period. A high level of parasitism was attained after one or more parasitoid generations in mid-September. The superparasitism was observed after mid-September when the parasitoid attained extremely high density, and resulted in an increase in the proportion of males, high mortality, and a decrease in the size of the progeny.     

Dispersal and foraging behaviour of Platygaster californica: hosts can't run, but they can hide

Abstract.  1. Host–parasitoid models often identify foraging behaviour and dispersal distance as important for system persistence.
2. Laboratory observations and field trials were used to characterise foraging behaviour and dispersal capability of Platygaster californica Ashmead (Platygasteridae), a parasitoid of the gall midge Rhopalomyia californica Felt (Cecidomyiidae).
3. Although foraging parasitoids meticulously searched plants in laboratory observations, none of the laboratory trials resulted in 100% parasitism, and the proportion of parasitism declined as midge egg density increased.
4. The field trials showed that the distribution of parasitism over distance from a central release point was hump-shaped, as predicted by a simple diffusion model. Mean parasitoid dispersal distance was 4.5 m, considerably farther than the 1.7 m mean midge dispersal found in previous work.
5. Although the parasitoid appears to search thoroughly for midge eggs and to disperse farther than the midge, the results of this study show how this host–parasitoid system may persist due to spatially variable incomplete parasitism.     

Associational resistance mediated by natural enemies

Abstract.  1. Associational resistance theory suggests that the association of herbivore-susceptible plant species with herbivore-resistant plant species can reduce herbivore density on the susceptible plant species. Several casual mechanisms are possible but none has so far invoked natural enemies. Associational resistance mediated by natural enemies was tested for by examining densities of a gall fly, Asphondylia borrichiae (Diptera: Cecidomyiidae), and levels of parasitism on two closely related seaside plants, Borrichia frutescens and Iva frutescens , when alone and when co-occurring.
2. Both Borrichia and Iva grow alone or together on small offshore islands in Florida. Each host plant species has its own associated race of fly, but both races of fly are attacked by the same four species of parasitoids. Borrichia normally has a higher density of galls than Iva , and galls are larger on Borrichia than on Iva .
3. Gall size, gall abundance, parasitism levels, and parasitoid community composition were quantified on both Borrichia and Iva on islands where each species grew alone or together. Some islands were then manipulated by adding Borrichia to islands supporting only Iva , and by adding Iva to islands supporting only Borrichia . Subsequent gall densities and gall parasitism levels on the original native species were then examined.
4. On both natural and experimentally manipulated islands, gall densities on Iva were significantly lowered by the presence of Borrichia . This is because bigger parasitoid species that were common on Borrichia galls, which are bigger, spilled over and attacked the smaller Iva galls. Thus, parasitism rates on Iva were higher on islands where Borrichia co-occurred than on islands where Borrichia were absent. Most parasitoids from Iva were too small to successfully attack the large Borrichia galls and so gall density on Borrichia was unaffected by the presence of Iva .     

Host refuges and spatial patterns of parasitism in an endophytic host–parasitoid system

Abstract. 1. Larvae of Tephritis conura Loew (Diptera: Tephritidae) live gregariously in flower heads of Cirsium heterophyllum (L.) Hill (Cardueae). They are attacked by the endoparasitic wasps Eurytoma sp. near tibialis Boheman (Hymenoptera: Eurytomidae) and Pteromalus caudiger (Graham) (Hymenoptera: Pteromalidae).
2. The responses of the parasitoids to different host patch sizes were investigated from the analysis of field samples. At the host population level, overall probabilities of parasitism were independent of host numbers per flower head or showed a tendency to inverse density-dependence for both parasitoid species.
3. Measurements of ovipositor length in Eurytoma and P.caudiger indicated that parts of the flower head constitute a structural refuge from parasitism.
4. The accessibility of hosts in a flower head was found to differ markedly, depending on larval locations and flower head characters. In spite of this high variability, similar average percentages of larvae were accessible to the parasitoids in each patch size class.
5. High variability of oviposition success in laboratory experiments can be explained by random locations of hosts in the flower heads.     

Gall size determines the structure of the Rabdophaga strobiloides host–parasitoid community

Abstract.  1. The relationship between gall size and mortality of the willow pinecone gall midge Rabdophaga strobiloides (Diptera: Cecidomyiidae) was examined by determining the fate of all galls in a 30-ha area in central Alberta, Canada over 4 years. It was found that gall size has a large effect on the type and intensity of mortality experienced by the gall midge, and consequently this factor has the potential to influence the dynamics of the host–parasitoid interaction through the creation of phenotypic refuges.
2. Total midge mortality ranged from 51% to 78% over the course of the study and was dominated by parasitism by Torymus cecidomyiae (Hymenoptera: Torymidae) and Gastrancistrus sp. (Hymenoptera: Pteromalidae) as well as predation by birds. Gall size had a strong, non-linear effect on the attack rates of each of these natural enemies.
3. Birds attacked the smallest size classes. Torymus cecidomyiae preferentially attacked medium diameter galls and thus avoided predation by birds in smaller galls. Gastrancistrus sp. preferentially attacked the largest galls and consequently suffered lower rates of predation by both T. cecidomyiae and birds.
4. This study emphasises the importance of understanding the interactions among mortality factors in order to describe adequately the susceptibility of R. strobiloides to parasitism and predation, and ultimately its population dynamics.     

Spatial and temporal variation in the parasitoid assemblage of an exophytic polyphagous caterpillar

Abstract 1. Over 3400 larvae of the polyphagous ground dwelling arctiid Grammia geneura were sampled and reared over seven generations in order to characterise its parasitoid assemblage and examine how and why this assemblage varies over time and space at a variety of scales.
2. The total parasitoid assemblage of 14 species was dominated both in diversity and frequency by relatively polyphagous tachinid flies.
3. Both the composition of the parasitoid assemblage and frequency of parasitism varied strikingly among and within sampling sites, seasons, and years.
4. Overall rates of parasitism increased consistently over the duration of caterpillar development.
5. Within sampling sites, parasitism rates were non-random with respect to habitat structure and caterpillar behaviour for the most abundant parasitoid species.
6. The large variability in parasitoid assemblage structure over space and time in this system may be a function of local host population abundance, habitat-specific parasitism, and indirect interactions between G. geneura and other Macrolepidoptera through shared oligophagous and polyphagous parasitoids.     

Cannibalism of parasitoid‐attacked conspecifics in a non‐carnivorous caterpillar

Cannibalism, the killing and consumption of conspecifics, can even occur in insect species typically considered to be non‐carnivorous. Of particular interest is the cannibalism of parasitoid‐attacked conspecifics, which could reduce parasitism levels in subsequent generations for that conspecific population. This study reports on the occurrence and some of the consequences of cannibalism in parasitoid‐attacked obliquebanded leafroller, Choristoneura rosaceana (Harris) (Lepidoptera: Tortricidae). We show that larvae of C. rosaceana, which is considered to be an herbivorous caterpillar species, did not prey upon live conspecifics, but readily consumed conspecifics attacked by Habrobracon gelechiae Ashmead (Hymenoptera: Braconidae). Further examination found that C. rosaceana larvae feeding on parasitoid‐attacked conspecifics, since their fourth instar, suffered a higher mortality and reduction in body size than those fed on plant material only. The cannibalism of attacked conspecifics did not appear to offer any nutrient benefits for the cannibal. To our best knowledge, this is the first empirical example of the occurrence and some of the consequences of cannibalism by a non‐carnivorous insect on its parasitoid‐attacked conspecifics. We discuss the adaptive significance of such cannibalism on parasitoid‐attacked conspecifics with respect to a trans‐generational fitness gain for the population through the killing of the parasitoids, thereby reducing parasitism in subsequent generations.     

Leptidea sinapis (Wood White butterfly) egg-laying habitat and adult dispersal studies in Herefordshire

The Wood White butterfly Leptidea sinapis, a UK BAP Priority species, is present in a number of Forestry Commission woodlands in the West Midlands and these constitute an important part of the national resource of this butterfly. A joint SITA Trust funded project between the Forestry Commission and Butterfly Conservation (linking with the National Wood White Conservation Project) is researching the use of habitat by Leptidea sinapis within these sites with regard to targeting conservation management. Two aspects of this research are presented: the results of a mark-recapture study and an analysis of egg-laying habitat. Mark-recapture results show considerable movement between areas of concentrations of adults and between egg-laying areas, with males moving further and faster than females. Movements do occur across potential habitat barriers. Egg locations were found by following females and by searching for eggs. The habitat used for egg-laying is extremely variable even within a site. A number of foodplants species are used and habitat ranges from low height foodplants within bare ground to a foodplant height of over 1 m within thick vegetation and scrub. These results are being integrated into an ongoing project to restore Leptidea sinapis habitat within managed Forestry Commission woodlands.