Wilf Powell

Endoparasitism in cereal aphids: molecular analysis of a whole parasitoid community

Insect parasitoids play a major role in terrestrial food webs as they are highly diverse, exploit a wide range of niches and are capable of affecting host population dynamics. Formidable difficulties are encountered when attempting to quantify host–parasitoid and parasitoid–parasitoid trophic links in diverse parasitoid communities. Here we present a DNA‐based approach to effectively track trophic interactions within an aphid–parasitoid food web, targeting, for the first time, the whole community of parasitoids and hyperparasitods associated with a single host. Using highly specific and sensitive multiplex and singleplex polymerase chain reaction, endoparasitism in the grain aphid Sitobion avenae (F) by 11 parasitoid species was quantified. Out of 1061 aphids collected during 12 weeks in a wheat field, 18.9% were found to be parasitized. Parasitoids responded to the supply of aphids, with the proportion of aphids parasitized increasing monotonically with date, until the aphid population crashed. In addition to eight species of primary parasitoids, DNA from two hyperparasitoid species was detected within 4.1% of the screened aphids, with significant hyperparasitoid pressure on some parasitoid species. In 68.2% of the hyperparasitized aphids, identification of the primary parasitoid host was also possible, allowing us to track species‐specific parasitoid‐hyperparasitoid links. Nine combinations of primary parasitoids within a single host were found, but only 1.6% of all screened aphids were multiparasitized. The potential of this approach to parasitoid food web research is discussed.

Reduced response of insecticide-resistant aphids and attraction of parasitoids to aphid alarm pheromone; a potential fitness trade-off

Response to the alarm pheromone, (E)-beta-farnesene, produced by many species of aphids, was assessed in laboratory bioassays using an aphid pest, Myzus persicae (Sulzer), and its primary endoparasitoid, Diaeretiella rapae (McIntosh). This was done in three separate studies, the first investigating responses of a large number of M. persicae clones carrying different combinations of metabolic (carboxylesterase) and target site (kdr) insecticide resistance mechanisms, and the other two investigating the responses of young virgin female adult parasitoids. In M. persicae, both insecticide resistance mechanisms were associated with reduced repellence suggesting that each has a pleiotropic effect on aphid behaviour. In contrast, D. rapae females were attracted to the alarm pheromone source. The implications of this apparent fitness trade-off for the evolution and dynamics of insecticide resistance, and the potential for using beneficial insects to combat resistance development are discussed.

Interference between parasitoids [Hym.: Aphidiidae] and fungi [Entomophthorales] attacking cereal aphids

In field populations of cereal aphids parasitism levels declined through the season as fungal infection increased. In laboratory trials the fungusErynia neoaphidis Remaudiere & Hennebert took 3 to 4 days to kill the rose-grain aphid,Metopolophium dirhodum (Walker), whereas the parasitoidAphidius rhopalosiphi De Stefani-Perez took 8 to 9 days at 20°C. When aphids were infected by the fungus less than 4 days after being parasitized the parasitoids were prevented from completing their development. Conversely, when infection occurred more than 4 days after parasitization development of the fungus was significantly impaired. There was no histological evidence that the fungus invaded the tissues of the parasitoid when both attacked the same aphid.Interference between parasitoids and fungal pathogens must be taken into account when estimating the impact of these mortality agents on pest populations.RésuméDans les populations naturelles des pucerons des céréales, le niveau du parasitisme par les Hyménoptères diminue en cours de saison, alors que celui des mycoses augmente. En essais de laboratoire, à 20°C, la mycose àErynia neoaphidis Remaudière et Hennebert tue en 3 à 4 jours le puceronMetopolophium dirhodum (Walker), tandis quil en faut 8 à 9 à lHyménoptère parasiteAphidius rhopalosiphi De Stefani-Perez. Quand les pucerons sont infectés par le champignon moins de 4 jours après avoir été parasités, les parasitoïdes sont incapables dachever leur développement. Par ailleurs, quand linfection se développe plus de 4 jours après lattaque du parasitoïde, le taux de pucerons mycosés est significativement plus faible. Lexamen histologique na pas mis en évidence lenvahissement des tissus du parasitoïde par le champignon quand lun et lautre sont présents dans le même puceron.La concurrence entre les parasitoïdes et les champignons pathogènes doit être prise en compte lors de lestimation de limpact de ces agents de mortalité sur les populations de ravageurs.

The effects of non‐host plant essential oil volatiles on the behaviour of the pollen beetle Meligethes aeneus

The use of semiochemicals for manipulation of the pollen beetle Meligethes aeneus (Fabricius) (Coleoptera: Nitidulidae) is being investigated for potential incorporation into a push‐pull control strategy for this pest, which damages oilseed rape, Brassica napus L. (Brassicaceae), throughout Europe. The response of M. aeneus to non‐host plant volatiles was investigated in laboratory assays to establish whether they have any effect on host plant location behaviour. Two approaches were used. First a novel, moving‐air bioassay using air funnels was developed to compare the response of M. aeneus to several non‐host plant essential oils. The beetles avoided the host plant flowers in the presence of non‐host volatiles, suggesting that M. aeneus uses olfactory cues in host location and/or acceptance. The results were expressed as ‘repellency values’ in order to compare the effects of the different oils tested. Lavender (Lavendula angustifolia Miller) (Lamiaceae) essential oil gave the highest repellency value. In addition, a four‐arm olfactometer was used to investigate olfactory responses, as this technique eliminated the influence of host plant visual and contact cues. The attraction to host plant volatiles was reduced by the addition of non‐host plant volatiles, but in addition to masking the host plant volatiles, the non‐host volatiles were avoided when these were presented alone. This is encouraging for the potential use of non‐host plants within a push‐pull strategy to reduce the pest colonisation of crops. Further testing in more realistic semi‐field and field trials is underway.

Response of the Aphid Parasitoid Aphidius funebris to Volatiles from Undamaged and Aphid-infested Centaurea nigra

Two issues have hindered the understanding of the ecology and evolution of volatile-mediated tritrophic interactions: few studies have addressed noncrop systems; and few statistical techniques have been applied that are suitable for the analysis of complex volatile blends. In this paper, we addressed both of these issues by studying the noncrop system involving the plant Centaurea nigra, the specialist aphid Uroleucon jaceae, and the parasitoid Aphidius funebris. In a Y-tube olfactometer, A. funebris was attracted to the odor from undamaged C. nigra, but preferred the plant–host complex (PHC) after 3xa0d of feeding by 200 U. jaceae over the undamaged plant, but not after three or 5xa0d of feeding by 50 U. jaceae. When aphids were removed, the initial preference for the damaged plant remained, but the final preference was not greater than for the undamaged plant. No qualitative differences were detected between the headspaces of C. nigra and the C. nigra–U. jaceae PHC. For quantitative analysis, we used a compositional approach, which treats each compound produced as part of a blend, and not as a compound released in isolation, thus allowing analysis of the relative contribution of each compound to the blend as a whole. With this approach, subtle increases and decreases of some green leaf volatiles and monoterpenoids on the third day of aphid infestation were detected. Mechanically damaged C. nigra had a volatile profile that differed from undamaged C. nigra and the PHC. One and 10xa0ng of (Z)-3-hexenyl acetate, and 10 or 100xa0ng of 6-methyl-5-hepten-2-one were attractive to the parasitoid when placed in solution on filter paper. A. funebris appears to be using a combination of chemical cues to locate host-infested plants.

Behavioural side-effects of insecticide resistance in aphids increase their vulnerability to parasitoid attack

Previous studies using the aphid Myzus persicae have shown that strong heritable variability in a defence behaviour, response to aphid alarm pheromone, is consistently associated with the possession of two insecticide resistance mechanisms. Insecticide-susceptible and -resistant aphids therefore provide the ideal biological material for testing the hypothesis that interactions with the third trophic level (parasitoids) can play a significant inhibitory role in the evolution of adaptive traits at the second trophic level (aphids), based on a fitness trade-off between resistance to insecticides and avoidance of parasitism through defence behaviour. Eight parthenogenetic M. persicae clones, representing different insecticide resistance genotypes, were exposed to alarm pheromone to confirm their level of response. Observations of these clones during periods of exposure to adult female parasitoids, Diaeretiella rapae, were then made in small-scale arenas in the presence and absence of measured amounts of alarm pheromone. Clones showing a consistently high alarm response (insecticide-susceptible forms) displayed a range of behaviours during and after parasitoid attack that were significantly associated with greater survival (avoidance of parasitism) compared with aphids showing a low alarm response (insecticide-resistant forms). Furthermore, this culminated in the latter suffering significantly higher levels of mummification. These data not only provide important empirical evidence that a normal (wild-type) high aphid alarm response reduces vulnerability to parasitoid attack but also represent the first example of insecticide resistance genes having negative pleiotropic effects on fitness by producing maladaptive behaviours in the context of selection imposed by a higher trophic level.

Effect of the Presence of a Nonhost Herbivore on the Response of the Aphid Parasitoid Diaeretiella rapae to Host-infested Cabbage Plants

The vast majority of studies of plant indirect defense strategies have considered simple tritrophic systems that involve plant responses to attack by a single herbivore species. However, responses by predators and parasitoids to specific, herbivore-induced, volatile blends could be compromised when two or more different herbivores are feeding on the same plant. In Y-tube olfactometer studies, we investigated the responses of an aphid parasitoid, Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae), to odors from cabbage plants infested with the peach-potato aphid Myzus persicae (Sulzer) (Homoptera: Aphididae), in both the presence and absence of a lepidopteran caterpillar, Plutella xylostella L. (Lepidoptera: Plutellidae). Female parasitoids chose aphid-infested plants over uninfested plants but did not distinguish between caterpillar-infested and uninfested plants. When given a choice between odors from an aphid-infested plant and those from a plant infested with diamondback moth larvae, they significantly chose the former. Furthermore, the parasitoids responded equally to odors from a plant infested with aphids only and those from a plant infested with both aphids and caterpillars. The results support the hypothesis that the aphid and the caterpillar induce different changes in the volatile profile of cabbage plants and that D. rapae females readily distinguish between the two. Furthermore, the changes to the plant volatile profile induced by the caterpillar damage did not hinder the responses of the parasitoid to aphid-induced signals.

Two-step learning involved in acquiring olfactory preferences for plant volatiles by parasitic wasps

Aphidius ervi is a parasitic wasp of several aphid species, including Acyrthosiphon pisum. This wasp is used as a biological control agent of its host aphid species in many regions of the world. Compared with responses to volatiles from intact plants, A.xa0ervi females respond to host-infested plant volatiles but not to nonhost-infested plant volatiles. Furthermore, we previously demonstrated that A.xa0ervi preferred host aphid-infested plant volatiles to volatiles from intact plants only when they had been exposed to the host aphid-infested plant volatiles during their developmental stages (larval to emergence stages). The results suggested that A.xa0ervi females learn the host-infested volatiles during their development and we tested this hypothesis in this study. Learning occurred in two steps: during the late larval to prepupal stages (the first learning stage) and during adult emergence (the second learning stage). Furthermore, wexa0observed specificity to the host plant volatiles in the two-step learning. The preference for host-infested plant volatiles was modified when the wasps had been exposed to host aphid-infested plant volatiles in the first stage and then exposed to nonhost aphid-infested plant volatiles in the second stage. When they were exposed to nonhost aphid-infested plant volatiles in the first stage, wasp preference for volatiles was not detected, irrespective of their exposure to either host or nonhost aphid-infested plants in the second stage. The ecological functions of the two-step learning are discussed.

Fitness trade-off in peach-potato aphids (Myzus persicae) between insecticide resistance and vulnerability to parasitoid attack at several spatial scales

Insecticide-resistant clones of the peach-potato aphid, Myzus persicae (Sulzer), have previously been shown to have a reduced response to aphid alarm pheromone compared to susceptible ones. The resulting vulnerability of susceptible and resistant aphids to attack by the primary endoparasitoid, Diaeretiella rapae (McIntosh), was investigated across three spatial scales. These scales ranged from aphids confined on individual leaves exposed to single female parasitoids, to aphids on groups of whole plants exposed to several parasitoids. In all experiments, significantly fewer aphids from insecticide-susceptible clones became parasitised compared to insecticide-resistant aphids. Investigations of aphid movement showed at the largest spatial scale that more susceptible aphids than resistant aphids moved from their inoculation leaves to other leaves on the same plant after exposure to parasitoids. The findings imply that parasitoids, and possibly other natural enemies, can influence the evolution and dynamics of insecticide resistance through pleiotropic effects of resistance genes on important behavioural traits.

Electrophysiological and behavioural responses of the pollen beetle, Meligethes aeneus, to volatiles from a non-host plant, lavender, Lavandula angustifolia (Lamiaceae)

A semiochemical based push-pull strategy for control of oilseed rape pests is being developed at Rothamsted Research. This strategy uses insect and plant derived semiochemicals to manipulate pests and their natural enemies. An important element within this strategy is an understanding of the importance of non-host plant cues for pest insects and how such signals could be used to manipulate their behaviour. Previous studies using a range of non-host plants have shown that, for the pollen beetle Meligethes aeneus (Coleoptera: Nitidulidae), the essential oil of lavender, Lavandula angustifolia (Lamiaceae), was the most repellent. The aim of this study was to identify the active components in L. angustifolia oil, and to investigate the behaviour of M. aeneus to these chemicals, to establish the most effective use of repellent stimuli to disrupt colonisation of oilseed rape crops. Coupled gas chromatography-electroantennography (GC-EAG) and gas chromatography-mass spectrometry (GC-MS) resulted in the identification of seven active compounds which were tested for behavioural activity using a 4-way olfactometer. Repellent responses were observed with (±)-linalool and (±)-linalyl acetate. The use of these chemicals within a push-pull pest control strategy is discussed.