Phenological responses in a sycamore–aphid–parasitoid system and consequences for aphid population dynamics: A 20 year case study

Species interactions have a spatiotemporal component driven by environmental cues, which if altered by climate change can drive shifts in community dynamics. There is insufficient understanding of the precise time windows during which inter‐annual variation in weather drives phenological shifts and the consequences for mismatches between interacting species and resultant population dynamics—particularly for insects. We use a 20 year study on a tri‐trophic system: sycamore Acer pseudoplatanus, two associated aphid species Drepanosiphum platanoidis and Periphyllus testudinaceus and their hymenopteran parasitoids. Using a sliding window approach, we assess climatic drivers of phenology in all three trophic levels. We quantify the magnitude of resultant trophic mismatches between aphids and their plant hosts and parasitoids, and then model the impacts of these mismatches, direct weather effects and density dependence on local‐scale aphid population dynamics. Warmer temperatures in mid‐March to late‐April were associated with advanced sycamore budburst, parasitoid attack and (marginally) D. platanoidis emergence. The precise time window during which spring weather advances phenology varies considerably across each species. Crucially, warmer temperatures in late winter delayed the emergence of both aphid species. Seasonal variation in warming rates thus generates marked shifts in the relative timing of spring events across trophic levels and mismatches in the phenology of interacting species. Despite this, we found no evidence that aphid population growth rates were adversely impacted by the magnitude of mismatch with their host plants or parasitoids, or direct impacts of temperature and precipitation. Strong density dependence effects occurred in both aphid species and probably buffered populations, through density‐dependent compensation, from adverse impacts of the marked inter‐annual climatic variation that occurred during the study period. These findings explain the resilience of aphid populations to climate change and uncover a key mechanism, warmer winter temperatures delaying insect phenology, by which climate change drives asynchronous shifts between interacting species.     

Tritrophic interactions between parasitoids and cereal aphids are mediated by nitrogen fertilizer

Host plant nutritional quality can directly and indirectly affect the third trophic levels. The aphid–parasitoid relationship provides an ideal system to investigate tritrophic interactions (as the parasitoids are completely dependent for their development upon their hosts) and assess the bottom up forces operating at different concentrations of nitrogen applications. The effects of varying nitrogen fertilizer on the performance of Aphidius colemani (V.) reared on Sitobion avenae (F.) and Aphidius rhopalosiphi (D.) reared on Rhopalosiphum padi (L.) were measured. Parasitism and percent emergence of parasitoids were positively affected by nitrogen fertilizer treatments while developmental duration (egg, larval, and pupal stages) was not affected by increasing nitrogen inputs. In males and females of both parasitoid species, adult longevity increased with the increasing nitrogen fertilizer. Hind tibia length and mummy weight of both parasitoid species increased with nitrogen fertilizer concentrations, as a result of larger aphids. This study showed that nitrogen application to the soil can have important consequences for aboveground multitrophic interactions.     

Influence of “protective” symbionts throughout the different steps of an aphid–parasitoid interaction

Microbial associates are widespread in insects, some conferring a protection to their hosts against natural enemies like parasitoids. These protective symbionts may affect the infection success of the parasitoid by modifying behavioral defenses of their hosts, the development success of the parasitoid by conferring a resistance against it or by altering life-history traits of the emerging parasitoids. Here, we assessed the effects of different protective bacterial symbionts on the entire sequence of the host-parasitoid interaction (i.e., from parasitoid attack to offspring emergence) between the pea aphid, Acyrthosiphon pisum, and its main parasitoid, Aphidius ervi and their impacts on the life-history traits of the emerging parasitoids. To test whether symbiont-mediated phenotypes were general or specific to particular aphid–symbiont associations, we considered several aphid lineages, each harboring a different strain of either Hamiltonella defensa or Regiella insecticola, two protective symbionts commonly found in aphids. We found that symbiont species and strains had a weak effect on the ability of aphids to defend themselves against the parasitic wasps during the attack and a strong effect on aphid resistance against parasitoid development. While parasitism resistance was mainly determined by symbionts, their effects on host defensive behaviors varied largely from one aphid–symbiont association to another. Also, the symbiotic status of the aphid individuals had no impact on the attack rate of the parasitic wasps, the parasitoid emergence rate from parasitized aphids nor the life-history traits of the emerging parasitoids. Overall, no correlations between symbiont effects on the different stages of the host–parasitoid interaction was observed, suggesting no trade-offs or positive associations between symbiont-mediated phenotypes. Our study highlights the need to consider various sequences of the host-parasitoid interaction to better assess the outcomes of protective symbioses and understand the ecological and evolutionary dynamics of insect–symbiont associations.     

Plant Species Loss Affects Life-History Traits of Aphids and Their Parasitoids

The consequences of plant species loss are rarely assessed in a multi-trophic context and especially effects on life-history traits of organisms at higher trophic levels have remained largely unstudied. We used a grassland biodiversity experiment and measured the effects of two components of plant diversity, plant species richness and the presence of nitrogen-fixing legumes, on several life-history traits of naturally colonizing aphids and their primary and secondary parasitoids in the field. We found that, irrespective of aphid species identity, the proportion of winged aphid morphs decreased with increasing plant species richness, which was correlated with decreasing host plant biomass. Similarly, emergence proportions of parasitoids decreased with increasing plant species richness. Both, emergence proportions and proportions of female parasitoids were lower in plots with legumes, where host plants had increased nitrogen concentrations. This effect of legume presence could indicate that aphids were better defended against parasitoids in high-nitrogen environments. Body mass of emerged individuals of the two most abundant primary parasitoid species was, however, higher in plots with legumes, suggesting that once parasitoids could overcome aphid defenses, they could profit from larger or more nutritious hosts. Our study demonstrates that cascading effects of plant species loss on higher trophic levels such as aphids, parasitoids and secondary parasitoids begin with changed life-history traits of these insects. Thus, life-history traits of organisms at higher trophic levels may be useful indicators of bottom-up effects of plant diversity on the biodiversity of consumers.     

Climate variation alters the synchrony of host–parasitoid interactions

Observed changes in mean temperature and increased frequency of extreme climate events have already impacted the distributions and phenologies of various organisms, including insects. Although some research has examined how parasitoids will respond to colder temperatures or experimental warming, we know relatively little about how increased variation in temperature and humidity could affect interactions between parasitoids and their hosts. Using a study system consisting of emerald ash borer (EAB), Agrilus planipennis, and its egg parasitoid Oobius agrili, we conducted environmentally controlled laboratory experiments to investigate how increased seasonal climate variation affected the synchrony of host–parasitoid interactions. We hypothesized that increased climate variation would lead to decreases in host and parasitoid survival, host fecundity, and percent parasitism (independent of host density), while also influencing percent diapause in parasitoids. EAB was reared in environmental chambers under four climate variation treatments (standard deviations in temperature of 1.24, 3.00, 3.60, and 4.79°C), while O. agrili experiments were conducted in the same environmental chambers using a 4 × 3 design (four climate variation treatments × 3 EAB egg densities). We found that EAB fecundity was negatively associated with temperature variation and that temperature variation altered the temporal egg laying distribution of EAB. Additionally, even moderate increases in temperature variation affected parasitoid emergence times, while decreasing percent parasitism and survival. Furthermore, percent diapause in parasitoids was positively associated with humidity variation. Our findings indicate that relatively small changes in the frequency and severity of extreme climate events have the potential to phenologically isolate emerging parasitoids from host eggs, which in the absence of alternative hosts could lead to localized extinctions. More broadly, these results indicate how climate change could affect various life history parameters in insects, and have implications for consumer–resource stability and biological control.     

Metapopulation dynamics in an aphid-parasitoid system

Metapopulation theory makes a number of predictions concerning the effects of dispersal on the persistence of predator-prey or host-parasitoid systems. While the stabilising effects of dispersal have been shown in a number of laboratory studies, evidence from field studies remains scarce due to a lack of suitable model systems. I describe a host-parasitoid system that shows a classical metapopulation structure with frequent extinctions and colonisations consisting of the aphidiid Lysiphlebus hirticornisand the aphid Metopeurum fuscoviride. Both the parasitoid and the aphid are specialists on their respective hosts. I followed the dynamics of host and parasitoid on individually marked tansy (Tanacetum vulgare) plants, the host of M. fuscoviride. Dynamics of host and parasitoid populations were characterized by frequent extinctions and colonisations. Mean longevity of aphid colonies was only 3.1 weeks. Parasitism by L. hirticorniswas a main cause of extinction for the aphid as rates of parasitism often reached 100%, in particular towards the end of the field season. Patchiness in this system occurs at two spatial scales. Aphid colonies form on single tansy ramets = shoots but movements of aphid individuals among ramets within a particular tansy genet are frequent. Because aphids can persist on a genet for a large numer of generations, it is argued that local populations form on genets rather than ramets. The number of host and parasitoid extinctions described in this study exceeds the number of extinctions usually observed in field studies of host-parasitoid metapopulations. It is suggested that aphid-parasitoid systems such as the one studied in this paper may be good models to test the predictions of metapopulation theory.     

Elevated air temperature alters an old-field insect community in a multifactor climate change experiment

To address how multiple, interacting climate drivers may affect plant–insect community associations, we sampled insects that naturally colonized a constructed old‐field plant community grown for over 2 years under simultaneous CO₂, temperature, and water manipulation. Insects were sampled using a combination of sticky traps and vacuum sampling, identified to morphospecies and the insect community with respect to abundance, richness, and evenness quantified. Individuals were assigned to four broad feeding guilds in order to examine potential trophic level effects. Although there were occasional effects of CO₂ and water treatment, the effects of warming on the insect community were large and consistent. Warming significantly increased Order Thysanoptera abundance and reduced overall morphospecies richness and evenness. Nonmetric multidimensional scaling found that only temperature affected insect community composition, while a Sørensen similarity index showed less correspondence in the insect community between temperature treatments compared with CO₂ or soil water treatments. Within the herbivore guild, elevated temperature significantly reduced richness and evenness. Corresponding reductions of diversity measures at higher trophic levels (i.e. parasitoids), along with the finding that herbivore richness was a significant predictor of parasitoid richness, suggest trophic‐level effects within the insect community. When the most abundant species were considered in temperature treatments, a small number of species increased in abundance at elevated temperature, while others declined compared with ambient temperature. Effects of temperature in the dominant insects demonstrated that treatment effects were limited to a relatively small number of morphospecies. Observed effects of elevated CO₂ concentration on whole‐community foliar N concentration did not result in any effect on herbivores, which are probably the most susceptible guild to changes in plant nutritional quality. These results demonstrate that climatic warming may alter certain insect communities via effects on insect species most responsive to a higher temperature, contributing to a change in community structure.     

Differential effects of flower feeding in an insect host–parasitoid system

In many insect host–parasitoid systems, both the host and its parasitoids forage on shared floral resources. As a result of insect behaviour, morphology and physiology, flower species may act selectively at different levels of such systems, e.g., between the trophic levels of hosts and parasitoids, between species within a guild, between sexes or individuals within a species or between life history traits within an individual. We asked if effects of selectivity are consistent across levels in the horse chestnut leafminer, Cameraria ohridella, and its parasitoid complex. Insects were exposed singly in no-choice feeding trials to twelve common flower species and their survival and reproduction were recorded. Only one of twelve flower species (Ranunculus acris) tended to selectively favour the longevity of leafminers, but not of parasitoids. No flower species were found to favour parasitoids only. Both trophic levels profited from feeding on Anthriscus sylvestris, however, parasitoids benefited up to eight times more than their hosts. No differences were found among the species of the parasitoid guild, but females lived significantly longer than males, and single individuals within species were able to exploit generally unfavourable flower species. Out of the seven flower species that increased the longevity of leafminer females, only Chaerophyllum hirsutum significantly enhanced the number of eggs laid. Fecundity was generally positively correlated with longevity of leafminer females, but two flower species (C. hirsutum, Taraxacum officinale) had an additional positive effect on fecundity. In conclusion, we demonstrated that flowers act differently on life history traits in a host–parasitoid system at a multitude of biological levels and that these effects are not always consistent across levels. Selective plant-derived resources can therefore modify herbivore–natural enemy interactions in ways that are more complex than currently appreciated.     

Climate change disproportionately increases herbivore over plant or parasitoid biomass

All living organisms are linked through trophic relationships with resources and consumers, the balance of which determines overall ecosystem stability and functioning. Ecological research has identified a multitude of mechanisms that contribute to this balance, but ecologists are now challenged with predicting responses to global environmental changes. Despite a wealth of studies highlighting likely outcomes for specific mechanisms and subsets of a system (e.g., plants, plant-herbivore or predator-prey interactions), studies comparing overall effects of changes at multiple trophic levels are rare. We used a combination of experiments in a grassland system to test how biomass at the plant, herbivore and natural enemy (parasitoid) levels responds to the interactive effects of two key global change drivers: warming and nitrogen deposition. We found that higher temperatures and elevated nitrogen generated a multitrophic community that was increasingly dominated by herbivores. Moreover, we found synergistic effects of the drivers on biomass, which differed across trophic levels. Both absolute and relative biomass of herbivores increased disproportionately to that of plants and, in particular, parasitoids, which did not show any significant response to the treatments. Reduced parasitism rates mirrored the profound biomass changes in the system. These findings carry important implications for the response of biota to environmental changes; reduced top-down regulation is likely to coincide with an increase in herbivory, which in turn is likely to cascade to other fundamental ecosystem processes. Our findings also provide multitrophic data to support the general concern of increasing herbivore pest outbreaks in a warmer world.     

Response of insect parasitism to elevation depends on host and parasitoid life-history strategies

How global warming will affect insect parasitoids and their role as natural enemies of insect pests is difficult to assess within a short period of time. Considering that elevation gradients can be used as analogues for global warming, we carried out meta-analyses of 27 correlations between parasitoid richness and elevation and 140 correlations between parasitism rate and elevation in natural and semi-natural environments. We also explored various covariates that may explain the observed responses. Both parasitism rates and parasitoid species richness significantly decreased with increasing elevation. The decrease was greater for ectoparasitoids and parasitoids of ectophagous insects than for endoparasitoids and parasitoids of endophagous hosts, possibly because these latter are better protected from adverse and extreme climatic conditions occurring at higher elevations. Although our results suggest an increase of parasitism with increasing temperature, other factors regulating herbivorous insects have to be considered before concluding that climate warming will lead to a decrease in pest density.     

Are aphid parasitoids from mild winter climates losing their winter diapause?

Temperature is both a selective pressure and a modulator of the diapause expression in insects from temperate regions. Thus, with climate warming, an alteration of the response to seasonal changes is expected, either through genetic adaptations to novel climatic conditions or phenotypic plasticity. Since the 1980s in western France, the winter guild of aphid parasitoids (Hymenoptera: Braconidae) in cereal fields has been made up of two species: Aphidius rhopalosiphi and Aphidius matricariae. The recent activity of two other species, Aphidius avenae and Aphidius ervi, during the winter months suggests that a modification of aphid parasitoid overwintering strategies has taken place within the guild. In this study, we first performed a field survey in the winter of 2014/15 to assess levels of parasitoid diapause incidence in agrosystems. Then, we compared the capacity of the four parasitoid species to enter winter diapause under nine different photoperiods and temperature conditions in the laboratory. As predicted, historically winter-active species (A. rhopalosiphi and A. matricariae) never entered diapause, whereas the species more recently active during winter (A. avenae and A. ervi) did enter diapause but at a low proportion (maximum of 13.4 and 11.2%, respectively). These results suggest rapid shifts over the last three decades in the overwintering strategies of aphid parasitoids in Western France, probably due to climate warming. This implies that diapause can be replaced by active adult overwintering, with potential consequences for species interactions, insect community composition, ecosystem functioning, and natural pest control.     

Host-parasitoid association and diffuse coevolution: when to be a generalist?

In host-parasitoid communities, hosts are subjected to selective pressures from numerous parasitoid species, and parasitoids may attack several host species. The specificity of host resistance and parasitoid virulence is thus a key factor in host-parasitoid coevolution. A continuum of strategies exists, from strict specificity to a generalist strategy. The optimal level of specificity may differ in host and parasitoid. I investigated the optimal level of resistance specificity using a model in which the host could be attacked by two parasitoid species, with variable levels of defense specificity. The fitness of a parasitoid attacking two host species with different levels of virulence specificity was also modeled. Finally, a fluctuating environment was simulated by introducing variable probabilities of encounters between antagonistic species over several generations. If the frequency of encounters with the antagonistic species is fixed, then both host and parasitoid gain from a strategy of exclusive specialization toward the most frequent antagonist. If the frequency of encounters fluctuates between generations, generalist host resistance and partially specialist parasitoid virulence are favored. Generalist host resistance may be considered to be a bet-hedging response to an unpredictable environment. This asymmetry in host-parasitoid coevolution may account for some of the genetic structures observed in the field for host-parasitoid associations.     

Overwintering strategies and cold hardiness of two aphid parasitoid species (Hymenoptera: Braconidae: Aphidiinae)

The role of winter diapause in two aphid parasitoid species, Aphidius ervi Haliday and Aphidius rhopalosiphi DeStefani-Peres (Hymenoptera: Braconidae: Aphidiinae), in host synchronization and the induction of cold hardiness was investigated. Parasitoids were reared during three successive generations on Sitobion avenae Fabricius, at 15 degrees C under a photoperiod of 9 h light 15 h dark. Although these conditions are known to be strongly diapause inducing, neither parasitoids showed an incidence of diapause above 65% over the three generations; the rest of the population underwent quiescence. In both parasitoid species, diapausing mummies exhibited greater cold hardiness than non-diapausing mummies, resulting in significantly lower supercooling points (SCP) and in a higher survival rate during long-term exposures at 0 and -10 degrees C. The induction of increased cold hardiness in parasitoids was thus associated with the diapause state. SCPs of third instar larvae of S. avenae were similar to those of non-diapausing mummies of both parasitoid species, but significantly higher than those of diapausing mummies. The effect of winter climate on the stability of the host-parasitoid interaction is discussed.     

Generalist predators disrupt parasitoid aphid control by direct and coincidental intraguild predation

Generalist predators and parasitoids are considered to be important regulators of aphids. The former not only feed on these pests, but might also consume parasitoids at all stages of development. This direct or coincidental interference affects the natural control of aphids, the scale of which is largely unknown, and it has rarely been examined under natural conditions. Here, molecular diagnostics were used to track trophic interactions in an aphid-parasitoid-generalist predator community during the build-up of a cereal aphid population. We found that generalist predators, principally carabid and staphylinid beetles as well as linyphiid spiders, had strong trophic links to both parasitoids and aphids. Remarkably, more than 50% of the parasitoid DNA detected in predators stems from direct predation on adult parasitoids. The data also suggest that coincidental intraguild predation is common too. Generalist predators, hence, disrupt parasitoid aphid control, although the levels at which the predators feed on pests and parasitoids seem to vary significantly between predator taxa. Our results suggest that taxon-specific trophic interactions between natural enemies need to be considered to obtain a more complete understanding of the route to effective conservation biological control.     

Trophic assimilation efficiency markedly increases at higher trophic levels in four-level host–parasitoid food chain

Trophic assimilation efficiency (conversion of resource biomass into consumer biomass) is thought to be a limiting factor for food chain length in natural communities. In host–parasitoid systems, which account for the majority of terrestrial consumer interactions, a high trophic assimilation efficiency may be expected at higher trophic levels because of the close match of resource composition of host tissue and the consumer''s resource requirements, which would allow for longer food chains. We measured efficiency of biomass transfer along an aphid-primary–secondary–tertiary parasitoid food chain and used stable isotope analysis to confirm trophic levels. We show high efficiency in biomass transfer along the food chain. From the third to the fourth trophic level, the proportion of host biomass transferred was 45%, 65% and 73%, respectively, for three secondary parasitoid species. For two parasitoid species that can act at the fourth and fifth trophic levels, we show markedly increased trophic assimilation efficiencies at the higher trophic level, which increased from 45 to 63% and 73 to 93%, respectively. In common with other food chains, δ¹⁵N increased with trophic level, with trophic discrimination factors (Δ¹⁵N) 1.34 and 1.49‰ from primary parasitoids to endoparasitic and ectoparasitic secondary parasitoids, respectively, and 0.78‰ from secondary to tertiary parasitoids. Owing to the extraordinarily high efficiency of hyperparasitoids, cryptic higher trophic levels may exist in host–parasitoid communities, which could alter our understanding of the dynamics and drivers of community structure of these important systems.     

Interactions of Russian wheat aphid, a hymenopterous parasitoid and resistant and susceptible slender wheatgrasses

Interactions among three trophic levels of resistant and susceptible slenderwheat grasses, Elymus trachycaulum (Link) Goule ex Shinners ex. H.F. Lewis, Russian wheat aphid, Diuraphis noxia (Mordvilko), and a hymenopterous parasitoid were studied in the laboratory and greenhouse. These relationships were compared with a commercial susceptible wheat Triticum aestivum L. variety. Aphids reared on the resistant entries showed significantly lower weights and numbers. Significant reduction of parasitoid mummy weight and adult size was positively correlated with the effects on the aphids. Resistant entries also induced a longer prereproductive period for both the aphids and parasitoids. Numbers of aphids and aphid damage were significantly modified by the addition of parasitoids. Parasitism was higher on plants that did not have leaf rolling. These findings may indicate that antibiosis resistance studied here is not the most desirable because it decreases natural enemy vitality.     

The influence of aphid-produced honeydew on parasitoid fitness and nutritional state: A comparative study

Honeydew is a sugar-rich resource excreted by many hemipteran species and is a key food source for other insect species such as ants and parasitoid wasps. Here, we evaluated the nutritional value of 14 honeydews excreted by 13 aphid species for the generalist aphid parasitoid Lysiphlebus testaceipes to test a series of hypotheses concerning variation in the nutritional value of honeydew. There was a positive correlation between the body sugar content of honeydew-fed parasitoids and their longevity. This information is valuable for biological control researchers because it demonstrates that the nutritional state of honeydew-fed parasitoids in the wild can indicate their fitness, independently of the honeydew source they have fed on.Although the carbohydrate content and longevity of L. testaceipes differed greatly among the different honeydews, we did not find a significant effect of aphid or host plant phylogeny on these traits. This result suggests that honeydew is evolutionarily labile and may be particularly subject to ecological selection pressures. This becomes apparent when considering host aphid suitability: Schizaphis graminum, one of the most suitable and commonly used hosts of L. testaceipes, produced honeydew of the poorest quality for the parasitoid whereas Uroleucon sonchi, one of the few aphids tested that cannot be parasitized by L. testaceipes, excreted the honeydew with the highest nutritional value. These data are consistent with the hypothesis that hemipterans are subject to selection pressure to minimize honeydew quality for the parasitoids that attack them.     

Food web structure of aphids and their parasitoids in Belgian fruit agroecosystems

Community structures of aphids and their parasitoids were studied in fruit crop habitats of eastern Belgium in 2014 and 2015. Quantitative food webs of these insects were constructed separately for each year, and divided into subwebs on three host‐plant categories, fruit crop plants, non‐crop woody and shrub plants and non‐crop herbaceous plants. The webs were analyzed using the standard food web statistics designed for binary data. During the whole study period, 78 plant species were recorded as host plants of 71 aphid species, from which 48 parasitoid species emerged. The community structure, aphid / parasitoid species‐richness ratio and trophic link number varied between the two years, whereas the realized connectance between parasitoids and aphids was relatively constant. A new plant–aphid–parasitoid association for Europe was recorded. Dominant parasitoid species in the study sites were Ephedrus persicae, Binodoxys angelicae and Praon volucre: the first species was frequently observed on non‐crop trees and shrubs, but the other two on non‐crop herbaceous plants. The potential influence, through indirect interactions, of parasitoids on aphid communities was assessed with quantitative parasitoid‐overlap diagrams. Symmetrical links were uncommon, and abundant aphid species seemed to have large indirect effects on less abundant species. These results show that trophic indirect interactions through parasitoids may govern aphid populations in fruit crop habitats with various non‐crop plants, implying the importance for landscape management and biological control of aphid pests in fruit agroecosystems.     

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.     

The influence of temperature on size as an indicator of host quality for the development of a solitary koinobiont parasitoid

The influence of aphid size on the host quality assessment and progeny performance of aphidiine parasitoids was examined using the mealy plum aphid parasitoid, Aphidius transcaspicus Telenga (Hymenoptera: Braconidae) and the black bean aphid, Aphis fabae Scopoli (Homoptera: Aphididae), as a readily acceptable alternate host. Aphid size in relation to stage of development was manipulated by rearing synchronous aphid cohorts at either 15 or 30 °C. At 15 °C, 2nd instar aphids were approximately the same size as 4th instar aphids reared at 30 °C. Cohorts of 30 aphids from each instar, reared at each temperature, were exposed to parasitism by a single parasitoid female for a period of 5 h. Overall susceptibility to parasitism did not vary between aphid cohorts, but the parasitoid response to aphid size differed significantly between rearing temperatures for both progeny sex ratio (parent female assessment of host quality) and larval growth and development (host suitability for parasitoid development). For aphids reared at 15 °C, the proportion of female progeny and emerging adult size for the parasitoid increased linearly with aphid size at the time of attack, while development time remained constant. In contrast, for aphids reared at 30 °C, the proportion of female progeny, emerging adult size, and the development time of the parasitoid all declined with aphid size at the time of attack. The contrasting responses of the parasitoid to host size for aphids reared at the two temperatures suggest that host quality is only indirectly related to aphid size among aphidiine parasitoids. The possible effects of higher temperatures on nutritional stress, obligate endosymbionts, and future growth potential of the aphids are discussed as explanations for the variation in host quality for parasitoid development.