A survey of aphids and aphid parasitoids in cereal fields in Denmark, and the parasitoids' role in biological control

In 1996 and 1997 a field survey of the abundance and species composition of cereal aphid primary and secondary parasitoids in spring barley, winter wheat and durum wheat was conducted in Zealand, Denmark. The purpose was to create a better understanding of the mechanisms underlying aphid–parasitoid dynamics in the field. Such an understanding can be used when developing biological control methods in cereals. In both years aphid attacks in cereals began in late June and never exceeded the economic threshold. In 1996 the first aphids were found in wheat on 26 June; in 1997 the first aphids were found on 24 June on both crops. The highest densities reached in 1996 were an average of six aphids per shoot in winter wheat and one aphid per shoot in spring barley. In 1997 the highest densities reached were 11 aphids per shoot in winter wheat and four aphids per shoot in spring barley. The aphid population collapsed by the end of July to early August in 1996, but it collapsed by mid-July in 1997. The onset and peak of parasitization were delayed in comparison to aphid infestation. Parasitism was 20–60% by the end of the cropping season in spring barley, and 30–80% in winter wheat and durum wheat in 1996. In 1997 parasitism did not exceed 3–11% in barley and was less than 2% in one winter wheat field but more than 40% in the other winter wheat field sampled. In both years most parasitism was due to Aphidiidae (Hymenoptera). The two dominant species were Aphidius ervi Haliday and Aphidius rhopalosiphi De Stefani-Perez. Hyperparasitism began after primary parasitism and increased progressively during the cropping season. The two years were similar in many respects, including for species composition of aphids and parasitoids. The late start of the aphid infestation may have contributed to the high level of parasitization found in 1996, but in 1997 the aphid infestation period was so short that a parasitoid population did not have time to build up.     

Plant virus and parasitoid interactions in a shared insect vector/host

Interactions between barley yellow dwarf luteovirus (BYDV) and the aphid parasitoid, Aphidius ervi Haliday (Hymenoptera: Aphidiidae), were investigated while sharing the vector/host, Sitobion avenae (F.) (Homoptera: Aphididae). Aphids, which were parasitized during their second larval stadium, had access to virus-infected plants before, immediately after, or several days after parasitoid attack. The larval development of A. ervi in S. avenae was significantly delayed when virus acquisition took place before or shortly after the parasitoid had hatched, but not when the parasitoid was at the second larval stage during virus acquisition. Similarly, the presence of BYDV led to a significantly higher aphid mortality when they acquired virus up to and including the time that A. ervi was at the first larval stage. Adult female parasitoids deposited fewer eggs in viruliferous aphids. Virus transmission was not reduced by parasitization, and in some experiments aphids which were subjected to parasitoid attack transmitted BYDV more efficiently than unattacked insects.     

The reactions of two cereal aphid parasitoids, Aphidius uzbekistanicus and A. ervi to host aphids and their food-plants

ABSTRACT. A Y-tube olfactometer was used to test the reactions of the hymenopteran cereal aphid parasitoids Aphidius uzbekistanicus Luzhetski and A. ervi Haliday to odours from aphids and their host plants. Only females responded to aphids but both sexes responded to plant odours. A. uzbekistanicus responded to the cereal aphids Sitobion avenae (F.) and Metopolophium dirhodum (Walker) whilst A. ervi , which has a broad host range, responded to M. dirhodum and the pea aphid, Acyrthosiphon pisum. Female A. uzbekistanicus responded to wheat leaves only but males responded to a range of plant material. Both male and female A. ervi responded to wheat and bean leaves. The failure of A. ervi to respond to either nettle aphids, Microlophium carnosum (Bukt.), or nettle leaves, despite its frequent parasitization of this aphid in the field, suggests the existence of more than one race of the parasitoid and casts doubts on the usefulness of alternative hosts as reservoirs for A. ervi in integrated control programmes. Males of both species responded to their respective females suggesting the presence of a sex specific attractant.     

Responses to aphid sex pheromones by the pea aphid parasitoids Aphidius ervi and Aphidius eadyi

Aphidius ervi and Aphidius eadyi, two parasitoids of the pea aphid Acyrthosiphon pisum, were attracted to components of the aphid sex pheromone in laboratory bioassays. Pre-test experience with host aphids in the presence of aphid sex pheromone did not affect the response of A. ervi to pheromone in a 4-way olfactometer, compared with that of naive parasitoids. Aphidius ervi females exposed only to the pheromone prior to testing did not respond in the olfactometer, suggesting habituation to the foraging cue by the parasitoid. In a wind tunnel, aphid sex pheromone increased the attraction of A. ervi to the plant-host complex (Vicia faba/A. pisum), suggesting an additive effect when two different foraging cues are present simultaneously.     

Complex interactions between a plant pathogen and insect parasitoid via the shared vector-host: consequences for host plant infection

Plant viruses modify the development of their aphid vectors by inducing physiological changes in the shared host plant. The performance of hymenopterous parasitoids exploiting these aphids can also be modified by the presence of the plant pathogen. We used laboratory and glasshouse microcosms containing beans (Vicia faba) as the host plant to examine the interactions between a plant virus (pea enation mosaic virus; PEMV) and a hymenopterous parasitoid (Aphidius ervi) that share the aphid vector/host Acyrthosiphon pisum. Neither PEMV-infection of V. faba, nor the carriage of PEMV virions by A. pisum, affected the growth or morphology of the aphid, or the oviposition behaviour and development of A. ervi. The presence of developing Aphidius ervi larvae within Acyrthosiphon pisum did not affect the ability of the aphids to transmit PEMV. However, by reducing their longevity, parasitism ultimately decreased the time viruliferous aphids were able to inoculate plants. In terms of virus dispersal, parasitized aphids exhibited more movement around experimental arenas than unparasitized controls, causing a slight increase in the proportion of beans infected with PEMV. Exposure to adult Aphidius ervi caused Acyrthosiphon pisum to rapidly drop off bean plants and disperse to new hosts, resulting in considerably higher plant infection rates (70%) than that seen in control arenas (25%). The results of this investigation demonstrate that when parasitoids are added to a plant-pathogen-vector system, benefits to the host plant due to reduced herbivore infestation must be balanced against the consequences of parasitoid-induced aphid dispersal and a subsequent increase in the level of plant infection.     

Phenology of Dasineura oxycoccana (Diptera: Cecidomyiidae) on cranberry and blueberry indicates potential for gene flow

Dasineura oxycoccana (Johnson) (Diptera: Cecidomyiidae) is a pest of cranberry, Vaccinium macrocarpon (Aiton) (Ericales: Ericaceae), and highbush blueberry, Vaccinium corymbosum (L.) (Ericales: Ericaceae), in North America. In British Columbia, Canada, D. oxycoccana was first found on highbush blueberry in 1991 and then on cranberry seven years later. Because many cranberry and highbush blueberry farms are adjacent to one another, we hypothesized that D. oxycoccana was moving from highbush blueberry onto cranberry. Cranberry and highbush blueberry differ in phenology, and adaptation to these different phenologies may result in host races or cryptic species on these two crops. We recognized the alternative hypothesis that D. oxycoccana had arrived as immature stages with cranberry vines imported from another region of North America. During spring and summer, we recorded the phenology of D. oxycoccana and the development of plant shoots from three cranberry and three highbush blueberry farms to determine whether the opportunity exists for successful movement of D. oxycoccana between the two crops. Our results show that D. oxycoccana from cranberry and highbush blueberry overlap in phenology for much of the season, indicating a high potential for movement and gene flow. However, differences were seen in number of larvae per shoot, location of pupae, and heat unit accumulation during larval development suggesting that instead there may be the potential for host race or cryptic species formation.     

Larval competition between Aphidius ervi and Praon volucre (Hymenoptera: Braconidae: Aphidiinae) in Macrosiphum euphorbiae (Hemiptera: Aphididae)

Interspecific competition between parasitoid larvae may influence the size, structure, and stability of the population, leading to a reduction in total parasitism and thus restricting the pest control. Aphidius ervi (Haliday) and Praon volucre (Haliday) are endoparasitoids that possess a wide host range and present considerable potential for the biological control of the aphid Macrosiphum euphorbiae (Thomas). The larval competition between A. ervi and P. volucre, and the possible intrinsic competitive superiority of one of the parasitoids in M. euphorbiae, have been studied. In single parasitism experiments, mated parasitoid females (n=10) were maintained individually in contact with M. euphorbiae hosts (n=30) inside petri dishes containing lettuce leaf discs and maintained in environmental chamber at 22 ± 1°C, 70 ± 10% RH, and 12-h photophase. The multiple parasitism experiments consisted of exposing single parasitized aphids (n=120) to the second parasitoid species. Two oviposition events were performed with a 4-h interval between them, namely the following: sequence A (oviposition by A. ervi, followed by P. volucre) and sequence B (oviposition by P. volucre, followed by A. ervi). Oviposition sequence A generated 24 A. ervi and 55 P. volucre adults, whereas oviposition sequence B generated 23 and 49 adults. P. volucre is an intrinsically superior competitor compared with A. ervi, and the use of the two species simultaneously may result in competitive exclusion and influence the stability of the parasitoid population.     

Potential effects of plant protease inhibitors, oryzacystatin I and soybean Bowman-Birk inhibitor, on the aphid parasitoid Aphidius ervi Haliday (Hymenoptera, Braconidae)

Protease inhibitors (PIs) have been shown to cause lethal and sublethal effects on aphids depending on the kind of PI and aphid species. Therefore, these proteins might affect aphid parasitoids directly by inhibiting their digestive proteolysis or indirectly via their development in a less suitable host. In our study, the risk of exposure and the potential effects of soybean Bowman-Birk inhibitor (SbBBI) and oryzacystatin I (OCI) on the aphid endoparasitoid Aphidius ervi were investigated using artificial diet to deliver PIs. Immunoassays showed that both SbBBI and OCI were detected in the honeydew of aphids reared on artificial diet containing these recombinant proteins at 100 microg/mL. However, only SbBBI was detected in parasitoid larvae, while this PI could not be detected in adult parasitoids emerged from PI-intoxicated aphids. Enzymatic inhibition assays showed that digestive proteolytic activity of larvae and adults of A. ervi predominantly relies on serine proteases and especially on chymotrypsin-like activity. Bioassays using SbBBI and OCI on artificial diet were performed. A. ervi that developed on intoxicated aphids had impaired fitness. Thus development and parasitism success of parasitoids exposed to OCI were severely affected. On the contrary, SbBBI only altered significantly female size and sex ratio. Direct exposure to PIs through adult food intake did not affect female's longevity, while SbBBI and OCI (100 microg/mL) induced 69% and 30% inhibition of digestive protease activity, respectively. These studies made it possible to estimate the risk of exposure to plant PIs and the sensitivity of the aphid parasitoid A. ervi to these entomotoxins, by combining immunological, biochemical and biological approaches. First it pointed out that only immature stages are affected by PIs. Secondly, it documented two different modes of effect, according to the nature of the PIs and both host and parasitoid susceptibility. OCI prevented the development of A. ervi mainly due to the host susceptibility, whereas SbBBI only induced sublethal effects on the parasitoid, possibly due to both direct action on the parasitoid susceptible proteases, and host-mediated action through size reduction.     

Host specialization in habitat specialists and generalists

Generalists and specialists use different cues to find their habitat and essential resources. While generalists have the advantage of exploiting a wider range of resources, they are predicted to be less efficient in using one particular resource compared to specialists. The level of specialization of parasitoids can be either at the habitat or at the host level; strategies used by either type are expected to differ. We examined interactions between three aphid parasitoid species that are a habitat specialist Aphidius rhopalosiphi, a habitat generalist Aphidius ervi, and a host generalist Praon volucre on three cereal aphids, Sitobion avenae, Metopolophium dirhodum and Rhopalosiphum padi. We compared total parasitism rate across behavioral and physiological variation in a non-choice test. Next, we addressed total parasitism in two phases to examine: (1) the response of parasitoids to different hosts through the behavioral sequence from antennation through oviposition, and (2) the physiological suitability of different hosts for oviposition and larval development. Parasitization typically involved the following behavioral steps: (1) antennal contact, (2) abdominal bending, and (3) ovipositor insertion (acceptance). A. rhopalosiphi had the same number of antennal contacts with the three aphids but showed fewer instances of abdominal bending towards R. padi. Pre-contact host preference was found for A. ervi but it did not correspond to the level of acceptance. The number of antennal contacts by P. volucre corresponded to the parasitization level of the aphid species but more mummies were produced on M. dirhodum than on R. padi. These results suggest that parasitoid species that are habitat specialists react similarly to the different host species present in the same habitat, whereas generalist species exhibit clear preferences during host selection. Preferences were, however, not always related to host suitability.     

Hopkins' 'host selection principle', another nail in its coffin

Abstract. Adult female parasitoids (Aphidius rhopalosiphi De Stef.) (Hymenoptera: Aphidiidae) reared on the aphid Metopolophium dirhodum (Walk.) (Homoptera: Aphididae) changed their responses to odours of two wheat cultivars ('Maris Huntsman' and 'Rapier') when the parasitized aphids had been moved from the former to the latter cultivar at various times after parasitization. If the aphids were moved after less than 6 days, the female parasitoids emerging from mummies by then formed on 'Rapier' responded positively to that cultivar, whereas parasitoids emerging from mummies transferred as still living aphids after 8 days on 'Maris Huntsman', responded positively to that cultivar rather than to 'Rapier' on which they had emerged. This appeared to be evidence for Hopkins' 'host selection principle', which states that chemical experience acquired by the larva of an endopterygote insect can be transferred through the pupal stage to the adult. However, discrimination in favour of either cultivar disappeared when the parasitoids were reared in aphids on both cultivars, and the emerging females were tested following excision of the pupae from the aphid mummies. The previous discrimination shown by adult parasitoids emerging from aphid mummies must therefore be determined by the chemicals contacted by a parasitoid on the skin of the mummy or while biting its way out of the dead aphid.     

Aphid clonal resistance to a parasitoid fails under heat stress

Parasitoid virulence and host resistance are complex interactions depending on metabolic rate and cellular activity, which in aphids additionally implicate heritable secondary symbionts among the Enterobacteriaceae. As performance of the parasitoid, the aphid host and its symbionts may differentially respond to temperature, the success or failure of aphid parasitism is difficult to predict when temperature varies. We tested the hypothesis that resistance of the pea aphid Acyrthosiphon pisum to the parasitoid Aphidius ervi, which is linked to aphid secondary symbionts, may depend on temperature in several resistant and non-resistant aphid clonal lineages of different geographic origin and of known bacterial symbiosis, using experiments in controlled environments. Complete immunity to A. ervi at 20 degrees C in three different aphid clones whose symbiosis is characterized by the possession of Hamiltonella defensa reversed to high susceptibility at 25 degrees C and especially 30 degrees C, suggesting that the aphid's immune responses to the establishment and early development of the parasitoid is strongly reduced at moderately high temperatures. There was no evidence that a pea aphid control genotype that was susceptible to A. ervi at 20 degrees C could become more resistant as temperature increases, as has been suggested for insect fungal pathogens. By contrast, our results suggest that aphid clonal resistance to A. ervi and related parasitoids is characteristic of cool temperature conditions, similar to various other fitness attributes of aphids. Based on evidence that H. defensa symbionts characterized all three A. ervi resistant pea aphid clones studied, but was absent in control aphids that remained susceptible at all temperatures, we suggest that secondary symbiosis plays a key role in the heat sensitivity of aphid clonal resistance. Our study may also indicate that aphid natural control of variably susceptible host populations by aphid parasitoids is more likely at moderate to high temperatures.     

Influence of the aphid pathogen Pandora neoaphidis on the foraging behaviour of the aphid parasitoid Aphidius ervi

Abstract.  1. The parasitoid Aphidius ervi and the entomopathogenic fungus Pandora neoaphidis both require successful invasion of an aphid host to complete their life cycle. A shorter developmental period allows P. neoaphidis to out-compete A. ervi. Aphidius ervi may reduce this fitness cost by avoiding aphid colonies containing P. neoaphidis . Here the response of A. ervi towards P. neoaphidis was assessed using sequential experiments designed to replicate different stages of parasitoid foraging behaviour.
2. Entry rate experiments showed that A. ervi entered aphid colonies containing P. neoaphidis -sporulating cadavers and that there was no significant difference in the attraction of A. ervi to aphid-damaged Vicia faba plants containing either healthy Acyrthosiphon pisum or P. neoaphidis -sporulating cadavers.
3. Observational behavioural experiments indicated that the presence of P. neoaphidis did not affect the search time or total foraging time of A. ervi on V. faba plants infested with either healthy A. pisum or P. neoaphidis -sporulating cadavers.
4. In Petri dish bioassays using aphids infected with P. neoaphidis over a period of 120 h, A. ervi showed no difference in attack rate against uninfected aphids or living aphids infected with P. neoaphidis for 1, 24, 48, 72, or 96 h. However, sporulating cadavers (120 h infection) were not attacked.
5.  Aphidius ervi appears only able to detect the presence of P. neoaphidis once the host is dead and sporulation has started. The fitness of A. ervi may therefore be severely reduced when foraging in P. neoaphidis -infected aphid colonies.     

Host castration by Aphidius ervi venom proteins

The braconid Aphidius ervi Haliday (Hymenoptera, Braconidae) is an endophagous parasitoid of the pea aphid, Acyrthosiphon pisum (Harris) (Homoptera, Aphididae). Parasitized host aphids show different degrees of castration, a response that is total when parasitoid oviposition takes place in first instar hosts. Deleterious effects on the host reproductive system are already evident by 24h following parasitization, before egg hatching. The effect of parasitoid venom on A. pisum ovaries has been studied by performing microinjections in non-parasitized host aphids and observing the cellular alterations of the apical germaria of ovarioles. Venom injection reproduced the same alterations observed in parasitized aphids, while injections of saline solution did not induce any detectable change. By 24h, the germarial cells of both venom-treated aphids and parasitized aphids showed the absence of the nucleolus and of electron-dense material around the nucleus, frequently referred to as "nuage material". By 48h more evident signs of degeneration were observed, suggesting the possible occurrence of apoptosis. The bioactive component of the venom was both heat- and protease-sensitive. The activity was found in purified fractions that were highly enriched in two proteins with an approximate molecular mass of 21kD and 36kD, respectively. These macromolecules are the most abundant components of A. ervi venom and, unlike many venom proteins of studied parasitic Hymenoptera, are not glycosylated and appear to be subunits of an oligomeric protein. The adaptive significance of host castration is discussed.     

Reactions of adult female parasitoids, particularly Aphidius rhopalosiphi, to volatile chemical cues from the host plants of their aphid prey

Abstract. In Y-tube olfactometer tests, Aphidius ervi Hal., Trioxys sp., Praon sp., Aphelinus flavus (Nees), Lysiphlebus fabarum (Marsh.) and Aphidius rophalosiphi De Stef. responded positively to the odour of the plant on which aphid mummies containing them had been collected. The response to host plant odour was greater than the response to the odour of host aphids, their honeydew or a combination of the two. The strongest response was to a combination of plant and host aphids. A. rhopalosiphi showed a strong positive response to three wheat volatiles (cis-3-hexenyl acetate, cis-3-hexen-1-ol and trans-2-hexenal) as well as to indole-3-acetaldehyde (a breakdown product of tryptophan in aphid honeydew). In both olfactometer tests with odours and choice trials with whole plants, newly emerged A. rhopalosiphi distinguished and preferred the variety of wheat on which their development had occurred to other wheat varieties.     

Snowdrop lectin (Galanthus nivalis agglutinin) in aphid honeydew negatively affects survival of a honeydew- consuming parasitoid

1 Insecticidal proteins can be excreted in the honeydew when sap-sucking insects feed on insect-resistant transgenic plants. Honeydew can be an important source of carbohydrates, thus potentially exposing a broad range of honeydew-feeding insects to transgene products.
2 Snowdrop lectin ( Galanthus nivalis agglutinin; GNA) dissolved in a 2 m sucrose solution had no antifeedant effect on female aphid parasitoids ( Aphidius ervi ) but had a direct negative effect on their longevity.
3 When feeding on honeydew from Rhopalosiphum padi feeding on a GNA-containing artificial diet, Aphidius ervi suffered a longevity reduction that was more pronounced than was to be expected based on the detected GNA concentration in the honeydew.
4 Analysis of carbohydrate and amino acid composition revealed that a change in honeydew composition caused by a GNA-effect on the aphids could be a possible explanation for the additional reduction in parasitoid longevity.
5 When comparing the effect of honeydew from Sitobion avenae and R. padi feeding on GNA-expressing or nontransformed wheat plants on A. ervi longevity, aphid species was found to have a significant effect, whereas the wheat variety had no effect. The latter result was probably due to low GNA expression levels in the plants. Differences in nutritional suitability between honeydew from R. padi and S. avenae could be explained by differences in carbohydrate and amino acid composition.
6 This is the first study to demonstrate that GNA ingested by aphids and transported into the honeydew can negatively affect the parasitoids consuming this honeydew.
7 We recommend that honeydew should be considered as a route of exposure to transgene products in future risk assessment studies.     

Effects of artificial diet containing GNA and GNA-expressing potatoes on the development of the aphid parasitoid Aphidius ervi Haliday (Hymenoptera: Aphidiidae)

Aphid parasitoids are important biological control agents. The possibility arises that whilst foraging on insect-resistant transgenic plants, they are themselves at risk from direct and indirect effects of the expression of a transgene used to control the pest species. A liquid artificial diet was successfully used to deliver the snowdrop lectin (Galanthus nivalis agglutinin; GNA) to the peach-potato aphid, Myzus persicae. Bioassays utilising artificial diet incorporating GNA, and excised leaves of the GNA-expressing transgenic potato line, GNA2#28, were performed to assess the potential effects of GNA on the development of the aphid parasitoid Aphidius ervi. The results indicate that GNA delivered via artificial diet to the aphids can be transferred through the trophic levels and has a dose-dependent effect on parasitoid development. Parasitoid larvae excreted most of the ingested GNA in the meconium but some of it was detected in the pupae. Although A. ervi development was not affected when developing within hosts feeding on transgenic potato leaves, this probably reflected sub-optimal expression of the toxin in the transgenic potato line used     

Evaluation of Vaccinium spp. for Illinoia pepperi (Hemiptera: Aphididae) performance and phenolic content

Host acceptance and population parameters of the aphid Illinoia pepperi (MacGillivray) (Hemiptera: Aphididae) were measured on highbush blueberry, Vaccinium corymbosum L. 'Elliott', and the wild species Vaccinium boreale Hall and Aalders, Vaccinium tenellum Aiton, Vaccinium pallidum Aiton, Vaccinium hirsutum Buckley, Vaccinium myrsinites Lamarck, and Vaccinium darrowi Camp. After 24 h of exposure, significantly fewer aphids remained in contact with V. boreale and V. hirsutum compared with V. corymbosum Elliott, V. darrowi, and V. pallidum. Length of the prereproductive period of I. pepperi was significantly longer on V. boreale and V. myrsinites, in contrast to V. corymbosum. Fecundity was also lower on V. boreale, V. hirsutum, V. myrsinites, and V. darrowi. Survivorship of I. pepperi 42 d after birth was significantly lower on V. hirsutum compared with the remaining Vaccinium spp. Reduced I. pepperi performance resulted in significantly lower intrinsic rate of increase (r(m)) values being associated with V. myrsinites, V. boreale, V. hirsutum, and V. darrowi, compared with V. corymbosum. Net reproductive rate (R(o)), generation time (T), and doubling time (T(d)) of I. pepperi also were affected by the Vaccinium spp. Total phenolic and flavonol content varied between Vaccinium spp., with some high phenolic content Vaccinium spp. having reduced aphid performance. However, no significant correlation between phenolics and I. pepperi performance was detected. Results from this study identified several potential sources of aphid resistance traits in wild Vaccinium spp.     

Variability and Parasitoid Foraging Efficiency: A Case Study of Pea Aphids and Aphidius ervi

When a parasitoid is searching for hosts, not all hosts are equally likely to be attacked. This variability in attack probability may affect the parasitoid functional response. Using a collection of experiments, we quantified the functional response of Aphidius ervi (Hymenoptera: Braconidae), an insect parasitoid of the pea aphid Acyrthosiphon pisum (Homoptera: Aphididae). We measured variability in the number of hosts attacked by a foraging parasitoid both among plants and within plants. At the first scale, A. ervi, searching among plants containing different numbers of aphids, showed both aphid-density-dependent and aphid-density-independent variability in the number of aphids attacked per plant. Within plants, A. ervi selectively attacked second and third instar aphids relative to other instars. Furthermore, there was variability in the susceptibility of attack among aphids independent of instar. Variability in attack rates among aphids both among and within plants decreased parasitoid foraging efficiency, with the greatest decrease caused by among-plant variability. Furthermore, the decrease in foraging efficiency was greatest when the average number of aphids per plant was low, thereby transforming a strong Type II functional response into one approaching Type I.     

Flying with a 'death sentence' on board: electrophoretic detection of braconid parasitoid larvae in migrating winged grain aphids, Sitobion avenae (F.)

Polyacrylamide gel electrophoresis of enzymes (carboxylesterases) was used for the first time to monitor rates of parasitism in airborne alate (winged) grain aphid, Sitobion avenae (F.) population samples collected by suction trapping in Hertfordshire, UK. Using previously described electrophoretic 'keys', the species of hymenopterous parasitoids present in individual aphids were identified and found to be Aphidius ervi (Haliday) and/or Aphidius rhopalosiphi (De Stephani Perez) (Braconidae). Entomophthoralean fungal infection was also detected using this approach. Aphidiid wasp parasitism was detected from early June to mid-August and fungal infection from late June to late July. The results are discussed in relation to parasitoid population structure and dynamics, especially (i) the fact that winged aphids passively transport the early stages of their braconid parasitoids and fungal pathogens, potentially to newly-founded colonies, which may directly impact on the dual aphid-parasitoid populations genetics; and (ii) the approach used to collect and assay parasitised and fungal infected aphids involving both suction trapping and electrophoretic testing may have potential in assessing the level and efficacy of these biological control agents in integrated pest management (IPM) schemes to combat cereal aphid outbreaks.     

Host handling and specificity of the hyperparasitoid wasp, Dendrocerus carpenteri (Curtis) (Hym., Megaspilidae): importance of host age and species

The oviposition behaviour of Dendrocerus carpenteri (Curtis), an ectophagous hyperparasitoid of aphidiine wasps inside mummified aphids was examined. Hyperparasitoids were provided in the laboratory with pea aphids ( Acyrthosiphon pisum ) which had been parasitized by three different species of aphidiine wasps ( Aphidius ervi, Ephedrus californicus and Praon pequodorum ) ranging in physiological age from the late larval stage to the late pupal stage. Females accepted only the hosts inside mummified aphids; they ignored live aphids, and did not accept dead, but not yet mummified aphids, although the latter were sometimes probed with the ovipositor. Female behaviour in handling A. ervi or E. californicus mummies did not change with experience; handling and oviposition times were stereotypic. However, naive females needed experience to locate the cocoon of P. pequodorum and distinguish it from the empty aphid mummy. Host acceptance and specificity were influenced more by the developmental stage than the species of the primary parasitoid. In dichotomous choice tests, hyperparasitoids 'preferred' prepupae over younger pupae of A. ervi , but they did not distinguish between these stages of E. californicus; older pupae were accepted at a low rate. Host preference was not influenced by conditioning on the rearing host. We consider several constraints on the host range of D. carpenteri , and discuss alternative explanations of differential hyperparasitism in the field.