Can hyperparasitoids cause large‐scale outbreaks of insect herbivores?

Synchronous population fluctuations occur in many species and have large economic impacts, but remain poorly understood. Dispersal, climate and natural enemies have been hypothesized to cause synchronous population fluctuations across large areas. For example, insect herbivores cause extensive forest defoliation and have many natural enemies, such as parasitoids, that may cause landscape‐scale changes in density. Between outbreaks, parasitoid‐caused mortality of hosts/herbivores is high, but it drops substantially during outbreak episodes. Because of their essential role in regulating herbivore populations, we need to include parasitoids in spatial modelling approaches to more effectively manage insect defoliation. However, classic host‐parasitoid population models predict parasitoid density, and parasitoid density is difficult to relate to host‐level observations of parasitoid‐caused mortality. We constructed a novel model to study how parasitoids affect insect outbreaks at the landscape scale. The model represents metacommunity dynamics, in which herbivore regulation, colonisation and extinction are driven by interactions with the forest, primary parasitoids and hyperparasitoids. The model suggests that parasitoid spatial dynamics can produce landscape‐scale outbreaks. Our results propose the testable prediction that hyperparasitoid prevalence should increase just before the onset of an outbreak because of hyperparasitoid overexploitation. If verified empirically, hyperparasitoid distribution could provide a biotic indicator that an outbreak will occur.     

Effects of environmental stress cascade up through four trophic levels in a salt marsh study system

1. Although in recent years there have been a number of studies demonstrating trophic cascades in terrestrial systems, it is still unclear what environmental conditions enable or enhance such cascades, especially among four trophic levels. 2. In this study, the influence of environmental stress (increased soil pore water salinity) on a four trophic level study system in a Florida salt marsh was examined by experimentally increasing soil pore water salinity. Effects of increased salinity on the quality of the host plant, Batis maritima, were assessed, as were resulting effects on the lepidopteran herbivore Ascia monuste, and the primary parasitoids and hyperparasitoids of its caterpillars. 3. Increased salinity altered host‐plant quality, which subsequently affected the consumer species. These effects of altered plant quality cascaded up through the herbivore and primary parasitoid to the hyperparasitoid Hypopteromalus inimicus, influencing its density, sex ratio, body size, and initial egg load. 4. These results demonstrate how heterogeneity in environmental stress can result in effects that cascade up through four trophic levels. We suggest that such strong effects at higher trophic levels may be more likely in systems in which relationships are more specific and intimate such as those among hosts, parasitoids, and hyperparasitoids.     

Environmental thermal levels affect the phenological relationships between the chestnut gall wasp and its parasitoids

Studies of thermal level‐related asynchrony in a host–parasitoid relationship are necessary to understand the effects of climate change on new host–parasitoid interactions. In the Asian chestnut gall wasp Dryocosmus kuriphilus (Hymenoptera: Cynipidae) and its Chalcidoidea parasitoids, phenological synchrony is assumed to be weather‐dependent in a new area of expansion. To evaluate the effects of environmental thermal regimes on the host, a phenology model for different cynipid stages (larvae, pupae, adults, and adult emergence) and a host–parasitoid phenological estimator are developed in three chestnut fields during two successive growth seasons and subsequently validated in areas with chestnut fields at two different altitudes. Comparisons of the timings of the juvenile and adult stages with those of the parasitoid complex demonstrate that the shortest period of occurrence for cynipids within galls has negative effects on the host–parasitoid relationships at higher temperature levels, thereby increasing phenological asynchrony for some parasitoids species. Reducing the development time of pupae and adults decreases the likelihood of success for some parasitoid species at higher temperature levels. We also record the extension of the gall wasp development time (approximately 15 days) at higher altitudes (linked to a lower mean temperature of approximately 1.5 °C). These results highlight how parasitization on the new hosts is dependent on the host phenology and, in the present study, is limited by the short duration of the presence of the host in galls, which could explain the considerable differences in cynipid gall wasp parasitization recorded at different altimeters.     

Foraging behaviour at the fourth trophic level: a comparative study of host location in aphid hyperparasitoids

In studies of foraging behaviour in a multitrophic context, the fourth trophic level has generally been ignored. We used four aphid hyperparasitoid species: Dendrocerus carpenteri (Curtis) (Hymenoptera: Megaspilidae), Asaphes suspensus Walker (Hymenoptera: Pteromalidae), Alloxysta victrix (Westwood) (Hymenoptera: Alloxystidae) and Syrphophagus aphidivorus (Mayr) (Hymenoptera: Encyrtidae), to correlate their response to different cues with their ecological attributes such as host range and host stage. In addition, we compared our results with studies of primary parasitoids on the same plant–herbivore system. First, the olfactory response of females was tested in a Y‐tube olfactometer (single choice: plant, aphid, honeydew, parasitised aphid, aphid mummy, or virgin female parasitoid; dual choice: clean plant, plant with aphids, or plant–host complex). Second, their foraging behaviour was described on plants with different stimuli (honeydew, aphids, parasitised aphids, and aphid mummies). The results indicated that olfactory cues are probably not essential cues for hyperparasitoid females. In foraging behaviour on the plant, all species prolonged their total visit time and search time as compared to the control treatment (clean plant). Only A. victrix did not react to the honeydew. Oviposition in mummies prolonged the total visit time because of the long handling time, but the effect of this behaviour on search time could not be determined. No clear correlation between foraging behaviour and host stage or host range was found. In contrast to specialised primary aphid parasitoids that have strong fixed responses to specific kairomones and herbivore‐induced synomones, more generalist aphid hyperparasitoids seem to depend less on volatile olfactory stimuli, but show similarities with primary parasitoids in their use of contact cues while searching on a plant.     

With or without you: Effects of the concurrent range expansion of an herbivore and its natural enemy on native species interactions

Global climatic changes may lead to the arrival of multiple range‐expanding species from different trophic levels into new habitats, either simultaneously or in quick succession, potentially causing the introduction of manifold novel interactions into native food webs. Unraveling the complex biotic interactions between native and range‐expanding species is critical to understand the impact of climate change on community ecology, but experimental evidence is lacking. In a series of laboratory experiments that simulated direct and indirect species interactions, we investigated the effects of the concurrent arrival of a range‐expanding insect herbivore in Europe, Spodoptera littoralis, and its associated parasitoid Microplitis rufiventris, on the native herbivore Mamestra brassicae, and its associated parasitoid Microplitis mediator, when co‐occurring on a native plant, Brassica rapa. Overall, direct interactions between the herbivores were beneficial for the exotic herbivore (higher pupal weight than the native herbivore), and negative for the native herbivore (higher mortality than the exotic herbivore). At the third trophic level, both parasitoids were unable to parasitize the herbivore they did not coexist with, but the presence of the exotic parasitoid still negatively affected the native herbivore (increased mortality) and the native parasitoid (decreased parasitism rate), through failed parasitism attempts and interference effects. Our results suggest different interaction scenarios depending on whether S. littoralis and its parasitoid arrive to the native tritrophic system separately or concurrently, as the negative effects associated with the presence of the parasitoid were dependent on the presence of the exotic herbivore. These findings illustrate the complexity and interconnectedness of multitrophic changes resulting from concurrent species arrival to new environments, and the need for integrating the ecological effects of such arrivals into the general theoretical framework of global invasion patterns driven by climatic change.     

Intrinsic competition between primary hyperparasitoids of the solitary endoparasitoid Cotesia rubecula

1. In nature, competitive interactions occur when different species exploit similar niches. Parasitic wasps (parasitoids) often have narrow host ranges and need to cope with competitors that use the same host species for development of their offspring. When larvae of different parasitoid species develop in the same host, this leads to intrinsic and often contest competition. Thus far, most studies on intrinsic competition have focused on primary parasitoids. However, competition among primary hyperparasitoids, parasitic wasps that use primary parasitoids as a host, has been little studied. 2. This study investigated intrinsic competition between two primary hyperparasitoids, the gregarious Baryscapus galactopus and the solitary Mesochorus gemellus, which lay their eggs in primary parasitoid larvae of Cotesia rubecula, while those in turn are developing inside their herbivore host, Pieris rapae. The aims were to identify: (i) which hyperparasitoid is the superior competitor; and (ii) whether oviposition sequence affects the outcome of intrinsic competition. 3. The results show that B. galactopus won 70% of contests when the two hyperparasitoids parasitised the host at the same time, and 90% when B. galactopus oviposited first. When M. gemellus had a 48 h head start, the two hyperparasitoids had an equal chance to win the competition. This suggests that B. galactopus is an intrinsically superior competitor to M. gemellus. Moreover, the outcome of competition is affected by time lags in oviposition events. 4. In contrast to what has been reported for primary parasitoids, we found that a gregarious hyperparasitoid species had a competitive advantage over a solitary species.     

The ectoparasitization of Coleophora alticolella (Lepidoptera) in relation to its aititudinal distribution

Abstract. 1. The parasitization of the larvae of Coleophora alticolella . feeding on Juncus squarrosus , was investigated at a series of altitudes from 15 to 520m above sea-level in northern England during 1977 and 1978.
2. Six species of primary parasitoid and one hyperparasitoid were reared from this host. Five of the primary parasitoids were ectophagous; only two specimens of the endoparasitoid, Gonotypus melanostoma , were reared.
3. All of the parasitoid species were recorded at 15 m but fewer at sites of higher altitude. Only one species, Scambus brevicomis , was recorded above 305 m, and none above 395 m. The hyperparasitoid, Tetrastichus endemus, was present only at 15 m.
4. Percentage parasitization was highest at 15 m; it was reduced from 51% to only 2% between 215 and 305 m in 1978. There was an increase in host density over this altitudinal range.
5. Three species, Scambus brevicomis. Elachertus olivaceus and Euderus viridis , accounted for most of the parasitization, but their relative proportions vaned at different altitudes.
6. The sex-ratios of the parasitoids reared from Coleophora alticolella ranged from 3.2% females for Scambus brevicomis , which is considered to also use larger hosts, to 99.4% females for Elachertus olivaceus , which develops by thelytokous parthenogenesis.
7. Euderus viridis and Scambus brevicomis started to attack the Coleophora alticolella larvae at a later date at 245 m than at 15 m, but attack by Elachertus olivacats was not delayed at the higher site.     

An exotic parasitoid provides an invasional lifeline for native parasitoids

The introduction of an exotic species may alter food webs within the ecosystem and significantly affect the biodiversity of indigenous species at different trophic levels. It has been postulated that recent introduction of the brown marmorated stinkbug (Halyomorpha halys (Stål)) represents an evolutionary trap for native parasitoids, as they accept H. halys egg masses as a host but produce no viable progeny. Interspecific interactions between European egg parasitoid, Trissolcus cultratus (Mayr), and an Asian parasitoid, Trissolcus japonicus (Ashmead), were assessed by providing egg masses to T. cultratus at various time intervals following the initial parasitization by T. japonicus. The suitability of the host for the parasitoid development was re‐assessed by providing T. cultratus with fresh and frozen egg masses of various ages. The likelihood of T. cultratus being able to attack previously parasitized egg masses was determined by assessing the duration of egg mass guarding behavior by T. japonicus following parasitization. The results of experiments examining the interspecific interactions between a native European egg parasitoid, T. cultratus, and an Asian parasitoid, T. japonicus (a candidate for the biological control of H. halys), showed that the native species can act as facultative hyperparasitoid of the exotic one. Although this is only possible during certain stages of T. japonicus development, the presence of the introduced parasitoid may reduce the impact of the evolutionary trap for indigenous parasitoid species. There is a possibility that the occurrence of facultative hyperparasitism between scelionid parasitoids associated with stinkbugs is common. This resulting intraguild predation could promote conservation and stabilization of natural communities by impacting the diversity and population dynamics of native stinkbugs and their parasitoids (e.g., by allowing native parasitoids to avoid wasting reproductive effort on unsuitable hosts), or reduce success of biological control programs (e.g., by reducing the population size of the exotic parasitoids).     

Four‐level interactions: herbivore use of ferns and subsequent parasitoid–hyperparasitoid performance

Abstract 1. Variables affecting species at the ends of trophic chains may modify the success of members with which they do not directly interact. The majority of such examples involve three trophic levels, but hyperparasitoids provide an excellent opportunity to examine four‐level relationships. 2. The gregarious hyperparasitoid Aprostocetus sp. (Hymenoptera: Eulophidae) commonly attacks the primary parasitoid Alabagrus texanus (Hymenoptera: Braconidae), by far the commonest parasitoid of the moth Herpetogramma theseusalis (Lepidoptera: Crambidae). 3. Larvae of this moth feed on ferns of two families, sensitive fern Onoclea sensibilis (Dryopteridaceae) and marsh fern Thelypteris palustris (Thelypteridaceae), in the study area, an old field in Maine, U.S.A. 4. I test the hypotheses that the ferns indirectly affect the reproductive success of the hyperparasitoids and that the ferns produce similar effects at intermediate links. 5. The moths experienced similar success on the two ferns, and the primary parasitoid performed similarly on moths reared from both ferns. The hyperparasitoid parasitized similar proportions of the primary parasitoid from moths that fed on sensitive fern and marsh fern. 6. However, hyperparasitoid broods on primary parasitoids from moths feeding on marsh fern contained approximately one‐third more offspring, whose individuals were significantly larger than those from sensitive fern, even though their hosts’ sizes did not differ significantly. 7. An indirect effect, related to the primary producers, thus strongly affected Trophic Level 4 in the absence of a significant effect at intermediate levels. To the best of my knowledge, this relationship has not been previously reported in a multi‐year or field‐based study of a natural system.     

Plant‐mediated indirect effects and the persistence of parasitoid–herbivore communities

We have examined the effects of herbivore diversity on parasitoid community persistence and stability, mediated by nonspecific information from herbivore‐infested plants. First, we investigated host location and patch time allocation in the parasitoid Cotesia glomerata in environments where host and/or nonhost herbivores were present on Brassica oleracea leaves. Parasitoids were attracted by infochemicals from leaves containing nonhost herbivores. They spent considerable amounts of time on such leaves. Thus, when information from the plant is indistinct, herbivore diversity is likely to weaken interaction strengths between parasitoids and hosts. In four B. oleracea fields, all plants contained herbivores, often two or more species. We modelled parasitoid–herbivore communities increasing in complexity, based on our experiments and field data. Increasing herbivore diversity promoted the persistence of parasitoid communities. However, at a higher threshold of herbivore diversity, parasitoids became extinct due to insufficient parasitism rates. Thus, diversity can potentially drive both persistence and extinctions.     

Comparing and contrasting life history variation in four aphid hyperparasitoids

1. In primary parasitoids, significant differences in life history and reproductive traits are observed among parasitoids attacking different stages of the same host species. Much less is known about hyperparasitoids, which attack different stages of primary parasitoids. 2. Parasitoids exploit hosts in two different ways. Koinobionts attack hosts that continue feeding and growing during parasitism, whereas idiobionts paralyse hosts before oviposition or attack non‐growing host stages, e.g. eggs or pupae. 3. Koino‐/idiobiosis in primary parasitoids are often associated with different expression of life history trade‐offs, e.g. endo‐ versus ectoparasitism, high versus low fecundity and short versus long life span. 4. In the present study, life history parameters of two koinobiont endoparasitic species (Alloxysta victrix; Syrphophagus aphidivorus), and two idiobiont ectoparasitic species (Asaphes suspensus; Dendrocerus carpenteri) of aphid hyperparasitoids were compared. These hyperparasitoids attack either the parasitoid larva in the aphid before it is killed and mummified by the primary parasitoid or the parasitoid prepupa or pupa in the dead aphid mummy. 5. There was considerable variation in reproductive success and longevity in the four species. The idiobiont A. suspensus produced the most progeny by far and had the longest lifespan. In contrast, the koinobiont A. victrix had the lowest fecundity. Other developments and life history parameters in the different species were variable. 6. The present results reveal that there was significant overlap in life history and reproductive traits among hyperparasitoid koinobionts and idiobionts, even when attacking the same host species, suggesting that selection for expression of these traits is largely association specific.     

Determinants of parasitoid communities of willow‐galling sawflies: habitat overrides physiology,host plant and space

Studies on the determinants of plant–herbivore and herbivore–parasitoid associations provide important insights into the origin and maintenance of global and local species richness. If parasitoids are specialists on herbivore niches rather than on herbivore taxa, then alternating escape of herbivores into novel niches and delayed resource tracking by parasitoids could fuel diversification at both trophic levels. We used DNA barcoding to identify parasitoids that attack larvae of seven Pontania sawfly species that induce leaf galls on eight willow species growing in subarctic and arctic–alpine habitats in three geographic locations in northern Fennoscandia, and then applied distance‐ and model‐based multivariate analyses and phylogenetic regression methods to evaluate the hierarchical importance of location, phylogeny and different galler niche dimensions on parasitoid host use. We found statistically significant variation in parasitoid communities across geographic locations and willow host species, but the differences were mainly quantitative due to extensive sharing of enemies among gallers within habitat types. By contrast, the divide between habitats defined two qualitatively different network compartments, because many common parasitoids exhibited strong habitat preference. Galler and parasitoid phylogenies did not explain associations, because distantly related arctic–alpine gallers were attacked by a species‐poor enemy community dominated by two parasitoid species that most likely have independently tracked the gallers’ evolutionary shifts into the novel habitat. Our results indicate that barcode‐ and phylogeny‐based analyses of food webs that span forested vs. tundra or grassland environments could improve our understanding of vertical diversification effects in complex plant–herbivore–parasitoid networks.     

Spatial and temporal diversity in hyperparasitoid communities of Cotesia glomerata on garlic mustard,Alliaria petiolata

1. Interactions between two trophic levels can be very intimate, often making species dependent on each other, something that increases with specialisation. Some specialised multivoltine herbivores may depend on multiple plant species for their survival over the course of a growing season, especially if their food plants are short‐lived and grow at different times. Later generations may exploit different plant species from those exploited by previous generations. 2. Multivoltine parasitoids as well as their natural enemies must also find their hosts on different food plants in different habitats across the season. Secondary hyperparasitoid communities have been studied on cocoons of the primary parasitoid, Cotesia glomerata (Hymenoptera: Braconidae), on black mustard (Brassica nigra) – a major food plant of its host, the large cabbage white (Pieris brassicae) – which grows in mid‐summer. 3. Here, hyperparasitoid communities on C. glomerata pupal clusters were studied on an early‐season host, garlic mustard, Alliaria petiolata, over ‘time’ (one season, April–July) in six closely located ‘populations’ (c. 2 km apart), and within two different ‘areas’ at greater separation (c. 100 km apart). At the plant level, spatial effects of pupal ‘location’ (canopy or bottom) on the plant were tested. 4. Although large‐scale separation (area) did not influence hyperparasitism, sampling time and small‐scale separation (population) affected hyperparasitism levels and composition of hyperparasitoid communities. Location on the plant strongly increased proportions of winged species in the canopy and proportions of wingless species in bottom‐located pupae. 5. These results show that hyperparasitism varies considerably at the local level, but that differences in hyperparasitoid communities do not increase with spatial distance.     

Trophic cascades in bell miner‐associated dieback forests: Quantifying relationships between leaf quality,psyllids and Psyllaephagus parasitoids

Coteries of the meliphagid bird Manorina melanophrys are associated with a form of eucalypt defoliation and recovery called bell miner‐associated dieback (BMAD). Through their defence of cooperative colony boundaries against other insectivorous birds, bell miners may foster greater abundances of lerp‐forming psyllids (Hemiptera: Aphalaridae), some of which reduce the lifespan of leaves. Trophic cascades in BMAD forests need to be understood to have a complete picture of regulatory processes. We studied relationships between leaf quality, psyllid and Psyllaephagus parasitoid/hyperparasitoid abundances within the Gondwana Rainforest World Heritage Area, NSW, Australia; our focal tree species were Eucalyptus propinqua and E. biturbinata. Eucalyptus biturbinata had tougher leaves than E. propinqua; leaf toughness of both species varied with site and tree. We found a statistically significant, negative relationship between toughness (surrogate for leaf age) and foliar nitrogen content; younger leaves had higher nitrogen contents. Both bell miner abundance and foliar nitrogen were positively correlated with psyllid abundance. The abundance of Glycaspis species (the psyllid that produces lerps with the highest sugar content) was more closely correlated with foliar nitrogen content than was the abundance of all five psyllid genera combined. We identified 14 Psyllaephagus spp./morphospecies, comprising 11 primary parasitoids and three hyperparasitoids. The abundance of all Psyllaephagus combined was positively correlated with the abundance of lerps. However, psyllid parasitism was not correlated with the abundance of lerps. The abundance of the three hyperparasitoids was positively correlated with the abundance of Psyllaephagus hosts. The availability of epicormic foliage (young, morphologically juvenile leaves produced following defoliation) is likely to alter the nutritional ecology underpinning the diversity and abundance of psyllid populations. Higher quality epicormic foliage should favour populations of Glycaspis species (by enhancing nymphal survival) creating lerp hotspots that induce residency by opportunistic bell miners. The positive contribution of induced amelioration, interacting with feedbacks from parasitoids and hyperparasitoids, to BMAD requires longitudinal investigation.     

Herbivore species identity rather than diversity of the non‐host community determines foraging behaviour of the parasitoid wasp Cotesia glomerata

Extensive research has been conducted to reveal how species diversity affects ecosystem functions and services. Yet, consequences of diversity loss for ecosystems as a whole as well as for single community members are still difficult to predict. Arthropod communities typically are species‐rich, and their species interactions, such as those between herbivores and their predators or parasitoids, may be particularly sensitive to changes in community composition. Parasitoids forage for herbivorous hosts by using herbivore‐induced plant volatiles (indirect cues) and cues produced by their host (direct cues). However, in addition to hosts, non‐suitable herbivores are present in a parasitoid's environment which may complicate the foraging process for the parasitoid. Therefore, ecosystem changes in the diversity of herbivores may affect the foraging efficiency of parasitoids. The effect of herbivore diversity may be mediated by either species numbers per se, by specific species traits, or by both. To investigate how diversity and identity of non‐host herbivores influence the behaviour of parasitoids, we created environments with different levels of non‐host diversity. On individual plants in these environments, we complemented host herbivores with 1–4 non‐host herbivore species. We subsequently studied the behaviour of the gregarious endoparasitoid Cotesia glomerata L. (Hymenoptera: Braconidae) while foraging for its gregarious host Pieris brassicae L. (Lepidoptera: Pieridae). Neither non‐host species diversity nor non‐host identity influenced the preference of the parasitoid for herbivore‐infested plants. However, after landing on the plant, non‐host species identity did affect parasitoid behaviour, whereas non‐host diversity did not. One of the non‐host species, Trichoplusia ni Hübner (Lepidoptera: Noctuidae), reduced the time the parasitoid spent on the plant as well as the number of hosts it parasitized. We conclude that non‐host herbivore species identity has a larger influence on C. glomerata foraging behaviour than non‐host species diversity. Our study shows the importance of species identity over species diversity in a multitrophic interaction of plants, herbivores, and parasitoids.     

Cascading effects of herbivore protective symbionts on hyperparasitoids

1. Microbial symbionts can play an important role in defending their insect hosts against natural enemies. However, researchers have little idea how the presence of such protective symbionts impacts food web interactions and species diversity. 2. This study investigated the effects of a protective symbiont (Hamiltonella defensa) in pea aphids (Acyrthosiphon pisum) on hyperparasitoids, which are a trophic level above the natural enemy target of the symbiont (primary parasitoids). 3. Pea aphids, with and without their natural infections of H. defensa, were exposed first to a primary parasitoid against which the symbiont provides partial protection (either Aphidius ervi or Aphelinus abdominalis), and second to a hyperparasitoid known to attack the primary parasitoid species. 4. It was found that hyperparasitoid hatch rate was substantially affected by the presence of the symbiont. This effect appears to be entirely due to the removal of potential hosts by the action of the symbiont: there was no additional benefit or cost experienced by the hyperparasitoids in response to symbiont presence. The results were similar across the two different aphid–parasitoid–hyperparasitoid interactions we studied. 5. It is concluded that protective symbionts can have an important cascading effect on multiple trophic levels by altering the success of natural enemies, but that there is no evidence for more complex interactions. These findings demonstrate that the potential influence of protective symbionts on the wider community should be considered in future food web studies.     

The influence of ant attendance on larval parasitism in hawthorn psyllids (Homoptera: Psyllidae)

The influence of ant attendance on parasitization of the larvae of three hawthorn psyllid species [Cacopsylla peregrina Förster, C. melanoneura Förster, C. crataegi (Schrank)] was studied over 2 years. All three psyllid species had low parasitization rates. However, the ant-attended C. crataegi was almost exclusively parasitized by Prionomitus mitratus (Dalman) (Hymenoptera: Encyrtidae) while the unattended C. peregrina and C. melanoneura were predominantly attacked by P. tiliaris (Dalman). Additionally, C. peregrina and C. melanoneura has significantly higher hyperparasitization rates than the ant-attended C. crataegi, with Pachyneuron muscarum as the dominant hyperparasitoid of all three psyllids. The mummies of C. peregrina and C. melanoneura were also heavily attacked by anthocorids. Both Prionomitus tiliaris and P. mitratus were disturbed and jumped away when encountering foraging ants. However, ant exclusion experiments showed that the primary parasitoid P. mitratus benefitted from ant attendance of its host C. crataegi as honeydew-collecting ants provided it with protection from hyperparasitoids.     

Population dynamics of Thecodiplosis japonensis (Diptera: Cecidomyiidae) under influence of parasitism by Inostemma matsutama and Inostemma seoulis (Hymenoptera: Platygastridae)

To understand influence of two species of parasitoids on host population dynamics, adult population dynamics of pine needle gall midge (PNGM), Thecodiplosis japonensis and two species of parasitoids, Inostemma matsutama and Inostemma seoulis were observed using emergence traps from 1986 to 2005. Density of PNGM decreased after outbreaks in 1986 and 1987 and showed density-dependent regulation. Relationships between density of PNGM and its parasitoids were linear except the period of outbreak regardless of parasitoids species. Relationships between host density and parasitism of I. matsutama and I. seoulis were density-independent and inverse density-dependent, respectively. I. seoulis was the dominant parasitoid against PNGM. Interspecific competition between two parasitoids was not strong and temporal niche segregation between two parasitoids was a possible mechanism for coexistence of two parasitoids. The parasitoid complex responded to changes in host density more sensitively than single parasitoid species. These results suggested that two parasitoid can stabilize PNGM population density without strong negative effects on each species of parasitoids.     

Establishment of <Emphasis Type="Italic">Psyllaephagus parvus</Emphasis> and <Emphasis Type="Italic">P. perplexans</Emphasis> as serendipitous biological control agents of Eucalyptus psyllids in southern California

The free-living lemon gum psyllid, Cryptoneossa triangula Taylor, and the lerp-forming spotted gum psyllid, Eucalyptolyma maideni Froggatt (Hemiptera: Psyllidae) are invasive pests of eucalypts in California. In 2007, Psyllaephagus parvus Riek (Hymenoptera: Encyrtidae) was discovered parasitizing spotted gum psyllids and Psyllaephagus perplexans Cockerell was collected from lemon gum psyllids. While neither parasitoid species was purposely introduced, presence of the parasitoids was significantly associated with reduced intensity and duration of population peaks for both psyllid species. Spring peaks were reduced more than fall peaks. We estimated minimum rates of parasitism from the ratio of mummies to live nymphs. Higher parasitism was recorded in coastal than inland locations during the spring, while parasitism was similar for coastal and inland populations in the fall. Logistic regression models suggest parasitoids were the determining factor of psyllid population densities, although physical parameters, such as irrigation, may affect psyllid or parasitoid populations.     

Native primary parasitoids and hyperparasitoids attacking an invasive aphid Uroleucon nigrotuberculatum in Japan

Since the invasion of Uroleucon nigrotuberculatum from North America we searched for parasitoids of this aphid on Solidago altissima in Japan to determine what species of native parasitoids attack the newly invasive aphid. We found three primary parasitoid species: Ephedrus plagiator and Praon yomenae (Braconidae, Aphidiinae) and Aphelinus albipodus (Aphelinidae). We also found eight hyperparasitoid species: Syrphophagus sp. (Encyrtidae), Dendrocerus carpenteri (Megaspilidae), Asaphes suspensus (Pteromalidae) and Pachyneuron aphidis (Pteromalidae) through both E. plagiator and A. albipodus; Phaenoglyphis villosa (Figitidae, Charipinae), Aprostocetus sp. (Eulophidae, Tetrastichinae) and D. laticeps through E. plagiator, and Alloxysta sp. nr brevis (Figitidae, Charipinae) through A. albipodus. Uroleucon nigrotuberculatum is usually attacked by rather polyphagous primary parasitoids, E. plagiator and A. albipodus, in Japan, where an oligophagous parasitoid specialized to allied aphid species is probably absent. The hyperparasitoid community of U. nigrotuberculatum is common to those of the aphids occurring in open field‐type habitats in Japan.