W. Powell

Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi

Herbivore induced release of plant volatiles mediating the foraging behavior of the aphid parasitoid Aphidius ervi was investigated using the pea aphid, Acyrthosiphon pisum, feeding on broad bean, Vicia faba. Behavioral responses were studied using an olfactometer and a wind tunnel. Volatiles obtained by air entrainment of aphid infested plants were more attractive to A. ervi than those from uninfested plants, in both behavioral bioassays. GC-EAG of both extracts showed a number of peaks associated with responses by A. ervi, but with some differences between extracts. Compounds giving these peaks were tentatively identified by GC-MS and confirmed by comparison with authentic samples on GC, using two columns of different polarity. The activity of pure compounds was further investigated by EAG and wind tunnel assays. Results showed that, of the compounds tested, 6-methyl-5-hepten-2-one was the most attractive for A. ervi females, with linalool, (Z)-3-hexen-1-yl acetate, (E)-β-ocimene, (Z)-3-hexen-1-ol, and (E)-β-farnesene all eliciting significantly more oriented flight behavior than a solvent control. Foraging experience significantly increased parasitoid responses to these compounds, with the exception of (E)-β-farnesene. Time-course GC analysis showed that feeding of A. pisum on V. faba induced or increased the release of several compounds. Release of two of these compounds (6-methyl-5-hepten-2-one and geranic acid) was not induced by the nonhost black bean aphid, Aphis fabae. During the analysis period, production of (E)-β-ocimene remained constant, but 6-methyl-5-hepten-2-one, linalool, geranic acid, and (E)-β-farnesene appeared during the first day after A. pisum infestation and increased in concentration with increasing time of aphid feeding.

Relative importance of semiochemicals from first and second trophic levels in host foraging behavior ofAphidius ervi.

The responses of femaleAphidius ervi to odors from a host food plant (Vicia faba), host aphids (Acyrthosiphon pisum), nonhost aphids (Aphis fabae), and aphid-plant complexes were investigated in a specially designed wind tunnel and a Y-tube olfactometer. In single-target (no-choice) and two-target (dual-choice) experiments, plant volatiles played a crucial role in the host foraging behavior ofA. ervi. The odor from theA. pisum-plant complex elicited the strongest responses byA. ervi females, followed by the odor from plants previously damaged by the feeding ofA. pisum. There was a significantly weaker response to odor fromA. pisum in the absence of the plant and to undamaged plants. Similarly, mechanically damaged plants and plants infested with the nonhost aphidA. fabae did not elicit strong responses. A plant that had been damaged byA. pisum and subsequently washed with distilled water was as attractive as an unwashed, previously infested plant.Aphidius ervi probably overcomes the reliability-detectability problem by selectively responding to herbivore-induced, volatile, semiochemical cues emitted by the first trophic level and by distinguishing between the volatiles induced by host and nonhost aphids.

Induction and Systemic Release of Herbivore-Induced Plant Volatiles Mediating In-Flight Orientation of Aphidius ervi

In-flight orientation of the braconid Aphidius ervi in response to volatiles released from broad bean plants infested by the pea aphid, Acyrthosiphon pisum, was studied in a no-choice wind-tunnel bioassay. The role of aphid infestation level and duration, systemic production of volatiles by “insect-free” parts of the plant, and the specificity of aphid-induced volatiles on the flight behavior of the foraging female parasitoids were investigated. The upper insect-free part of a three-leaved broad bean plant, which was basally infested by a population of 40 A. pisum, released synomones detectable by A. ervi females after at least 48–72 hr of infestation, resulting in both significant increases in oriented flights and landings on the source compared with uninfested control plants. This suggests that volatiles involved in host-location by A. ervi are systemically released by broad bean plants either in response to circulation of aphid saliva, circulation of saliva-induced bioactive elicitors, or circulation of the synomones themselves. Air entrainment extracts of volatiles collected from a broad bean plant infested by the nonhost Aphis fabae or an uninfested broad bean plant elicited few oriented flights and landing responses by female parasitoids. These extracts were significantly less attractive than extracts collected from a broad bean plant infested by the host A. pisum, indicating the specificity of synomones elicited by different aphid species on the same plant species.

The role of plant chemical cues in determining host preference in the generalist aphid parasitoid Aphidius colemani.

The host preference behaviour of the generalist aphid parasitoid Aphidius colemani was investigated using a Y‐tube olfactometer. Female A. colemani showed a preference for the host‐plant complex on which they had been reared, even though the same aphid host was involved, demonstrating a host plant preference. This preference was not evident when the parasitoids were dissected from their mummies prior to adult emergence. Host plant preference exhibited during host selection appeared to be induced by chemical cues encountered on the mummy case at the time of emergence, but preferences could be changed by subsequent foraging experiences. It is concluded that plant chemical cues play a major role in determining initial preferences through a process of emergence conditioning but that learning processes, involving cues encountered during oviposition in or contact with the host, can modify these initial preferences.

The relationship between primary parasitoids and hyperparasitoids of cereal aphids: an analysis of field data

1. We analysed data collected in 1983-89 from cereal fields to elucidate the relationships between the primary parasitoids and hyperparasitoids of cereal aphids. The analysis aimed to establish whether or not hyperparasitoids interfere with the impact of primary parasitoids on cereal aphid populations. 2. From more than 10000 parasitized aphids, 14 primary parasitoid and 18 hyperparasitoid species were reared. The five most common hyperparasitoids attacked the five most common primary parasitoids, which, in turn, parasitized most frequently the most abundant aphid species, Sitobion avenae (F.)

Chemically mediated associative learning in the host foraging behavior of the aphid parasitoid Aphidius ervi (Hymenoptera: Braconidae)

The effect of experience on the responsiveness of the braconid parasitoidAphidius ervi to host(Acyrthosiphon pisum)-associated cues was investigated on bean plants(Vicia faba) using a wind tunnel bioassay. Oviposition experience on the plant-host complex significantly increased the oriented flight and landing responses ofA. ervi females to an undamaged plant and to a plant-host(A. pisum) complex. However, oviposition experience onA. pisum aphids when isolated from the plant did not change their responses to the intact plant and the complex. Searching on an unwashed plant which had been previously damaged byA. pisum also increased their response to an undamaged plant and a host-damaged plant, whereas the experience of searching on an undamaged plant did not significantly change their responses to undamaged plants. However, when parasitoids were allowed to search on an undamaged plant which had been sprayed withA. pisum honeydew, this significantly increased their response to an undamaged plant. Oviposition experience on the plant-host complex and foraging experience on a host-damaged plant or an undamaged plant sprayed with honeydew also significantly reduced the mean time taken by the parasitoids to respond in the wind tunnel. The behavioral changes associated with such experience were acquired within 30 min and persisted for at least 3 days. The results demonstrate the capacity ofA. ervi to learn associatively olfactory cues from plants, host-damaged plants, and plant-host complexes and confirm the role of aphid honeydew as a host recognition kairomone forA. ervi.

The role of semiochemicals in the avoidance of the seven-spot ladybird, Coccinella septempunctata, by the aphid parasitoid, Aphidius ervi

The role of semiochemicals in mediating intraguild interactions between the seven-spot ladybird, Coccinella septempunctata, and the aphid parasitoid, Aphidius ervi, was investigated. Female parasitoids avoided leaves visited by C. septempunctata adults and larvae during the previous 24 hr. Ethanol extracts of C. septempunctata adults and larvae also induced avoidance responses by A. ervi. Two of the hydrocarbons identified by gas chromatography (GC) and coupled GC-mass spectrometry (GC-MS), n-tricosane (C23H48), and n-pentacosane (C25H52), when tested individually at levels found in the adult extract, induced avoidance by A. ervi. Further investigation of the larvae extract, and footprint chemicals deposited by adults in glass Petri dishes, confirmed the presence of the hydrocarbons. Parasitism rates of the pea aphid, Acyrthosiphon pisum, on broad bean plants, Vicia faba, which had been sprayed with a mixture of the chemicals, were lower than those on control plants. The effect, however, was no longer evident if parasitoid foraging was delayed by 24 hr after the plants were treated. The ecological significance of intraguild avoidance behavior and implications for possible use of the semiochemicals involved in future biological control programs are discussed.

Physical and chemical cues influencing the oviposition behaviour of Aphidius ervi.

The oviposition behaviour of the aphid parasitoid Aphidius ervi Haliday is influenced by both chemical and physical cues. Oviposition attack responses were elicited by paint pigments sealed into the tip of a glass capillary tube. Parasitoids reacted to yellow pigments with repeated oviposition attack responses, but they did not react to green pigments. The spectrum of reflected light from the yellow pigments was very similar to that from the ‘green’ natural host Acyrthosiphon pisum (Harris), with a high proportion of the total radiation energy being emitted in the yellow‐orange wavebands (580–660 nm). Pea aphid cornicle secretion also elicited oviposition attack responses, which were not exclusively induced by its pale yellow‐green colour. In fact, the oviposition attack response to capillary tips coated with cornicle secretion remained evident under red light conditions, which, in contrast, nearly completely suppressed the response to yellow pigments. Chemical compounds from cornicle secretion do not appear to be involved in parasitoid orientation, even though they stimulate intense oviposition attack responses. Olfactometer experiments showed that the putative kairomone involved acts only at very short range or on contact. Host exuviae, which also elicited strong and persistent oviposition reactions from A. ervi females, appear to be a good alternative source of ovipositional kairomone(s). This work confirms the existence of an aphid cuticular kairomone.

The role of honeydew as an ovipositional stimulant for two species of syrphids

The influence of honeydew contamination on egg laying by the syrphids Episyrphus balteatus (Deg.) and Platycheirus albimanus (F.) on ears of wheat was investigated in a large laboratory flight cage. Artificially‐applied honeydew elicited oviposition by E. balteatus but not by Platycheirus albimanus. Episyrphus balteatus females landed more frequently on ears contaminated with honeydew than on clean ears, suggesting a response to honeydew volatiles. Honeydew from the rose‐grain aphid Metopolophium dirhodum and from the pea aphid Acyrthosiphon pisum stimulated E. balteatus to lay eggs, whereas honeydew from the nettle aphid Microlophium carnosum did not. The number of eggs laid by E. balteatus increased with increasing honeydew concentration. At low honeydew concentrations the presence of aphids increased oviposition by E. balteatus, but aphid presence had little effect on the number of eggs laid at high honeydew concentrations.

The abilities of the aphid parasitoids Aphidius ervi Haliday and A. rhopalosiphi De Stefani Perez (Hymenoptera: Braconidae) to transfer between different known host species and the implications for the use of alternative hosts in pest control strategies

A series of host-transfer trials using both laboratory-cultured and field-collected individuals of the aphid parasitoids Aphidius ervi Haliday and A. rhopalosiphi De Stefani Perez were done in order to clarify inconsistent results from several previous studies. A. ervi cultured on Acyrthosiphon pisum (Harris) produced very few mummies when confined with Microlophium carnosum (Buckton), whereas those cultured on M. carnosum produced as many mummies on A. pisum as they did on their original host. Mummy production was correlated with the attack rate of adult parasitoids on potential hosts. The production of mummies on M. carnosum by parasitoids reared on A. pisum was often greatly improved if their male parent had been reared on M. carnosum , suggesting that genotype strongly influences host preference. Aphidius rhopalosiphi from laboratory cultures produced significantly more mummies on Metopolophium dirhodum (Walker) than on Sitobion avenae (F.) regardless of their original host, but this preference was not shown by parasitoids from field populations. It is concluded that inadvertent selection occurs in laboratory cultures of aphid parasitoids as a result of low founder numbers, genetic drift and genetic bottlenecks and that this can strongly influence experimental results in biology and behaviour studies, which has important implications for biological control workers.