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.     

Infection with an insect virus affects olfactory behaviour and interactions with host plant and natural enemies in an aphid

Aphid ecology and population dynamics are affected by a series of factors including behavioural responses to ecologically relevant chemical cues, capacity for population growth, and interactions with host plants and natural enemies. Using the aphid Rhopalosiphum padi (L.) (Homoptera: Aphididae), we showed that these factors were affected by infection with Rhopalosiphum padi virus (RhPV). Uninfected aphids were attracted to odour of uninfected aphids on the host plant, an aggregation mechanism. However, infected aphids were not attracted, and neither infected nor uninfected aphids were attracted to infected aphids on the plant. Infected aphids did not respond to methyl salicylate, a cue denoting host suitability. Infected aphids were more behaviourally sensitive to aphid alarm pheromone, and left the host plant more readily in response to it. RhPV reduced the lifespan and population growth rate of the aphid. The predacious ladybird, Coccinella septempunctata (L.) (Coleoptera: Coccinellidae), consumed more infected aphids than uninfected aphids in a 24‐h period, and the aphid parasitoid Aphidius ervi Haliday (Hymenoptera: Aphidiidae) attacked more infected than uninfected aphids. However, the proportion of mummies formed was lower with infected aphids. The results represent further evidence that associated organisms can affect the behaviour and ecology of their aphid hosts.     

The cowpea aphid, shape Aphis craccivora, host plant odours and pheromones

Olfactometer experiments were conducted with apterae and alatae of the cowpea aphid, Aphis craccivora, Koch (Hom.:Aphidoidea). The occurrence of density dependent related pheromones and odour response to their host plant Vigna unguiculata was studied. Apterae responded with positive anemotaxis to air passed over both small groups of apterae and alatae (10 individuals) but negatively to air that passed over a bigger group (20 individuals). Alatae responded in the same way to groups of apterae but were repelled by alatae independent of the size of the group applied as odour source in the olfactometer, except when exposed to air passing ten alatae feeding on cowpea leaves. This may be due to interaction between aphid pheromones and host plant odour. Both apterae and alatae showed a general attraction to green plants and were also able to distinguish between other host plants and cowpea, which was the original host of the aphid clone used in the experiments. When attacked by aphids, the cowpea plant responded with a temporal increase in attractivity that reached a maximum after 48 h and had disappeared after one week.     

Discrimination of alarm pheromone (E)-β-farnesene by aphid odorant-binding proteins

OBPs have been recently demonstrated to be required for odour perception in insects and directly involved in odour discrimination. In aphids they might represent new interesting targets for the control of their population in agriculture. Based on sequence information available in the EST database, we have cloned four genes encoding odorant-binding proteins (OBP) in Acyrthosiphon pisum and homologous genes in other aphid species. Unlike OBPs from other orders of insects, that are greatly divergent, in aphids these proteins have been found to be highly conserved, with differences between species limited to only few amino acid substitutions. On the contrary, similarities between OBP sequences of the same species are poor with 31% or less of identical amino acids. Three selected OBPs (OBP1, OBP3 and OBP8) have been expressed in bacteria and purified. Ligand-binding experiments have shown similar behaviour of the three proteins towards several organic compounds, but also some significant selectivities. In particular, (E)-β-farnesene, the alarm pheromone and its related compound farnesol exhibited good affinity to OBP3, but did not bind the other two proteins. We suggest that OBP3 could mediate response of aphids to the alarm pheromone.     

Odour-conditioned anemotaxis of apterous aphids (Cryptomyzus korschelti) in response to host plants

ABSTRACT. Orientation responses of adult apterous virginoparae of Cryptomyzus korschelti Börner were recorded using a locomotion-compensator in front of a wind tunnel. Individual aphids were tested under four consecutive treatments: without wind; clean wind; and wind carrying odour of the host plant Stachys sylvatica or odour of a non-host plant Solanum tuberosum. The walking tracks were tortuous in all treatments except when the odour of host plants was used. Host plant odour induced upwind orientation of aphids (odour-conditioned positive anemotaxis). Track variables such as vector length, straightness, upwind time and upwind length, increased when the aphids moved upwind. Walking speeds were not affected. The simultaneous stimulation by wind and host plant odour caused aphids to walk upwind for more than 1 m in 10 min. These findings suggest that olfactory attraction of aphids is involved in host plant selection.     

Herbivore-induced emissions of maize volatiles repel the corn leaf aphid, shape Rhopalosiphum maidis

When maize plants, Zea mays L., are mechanically damaged and the damaged sites are treated with caterpillar regurgitant, the plants will release a specific blend of volatiles. It is known that these volatiles can be attractive to natural enemies of herbivores. We hypothesise that the plant volatiles constitute part of the induced plant defence and that herbivores will be affected by the odours as well. In laboratory and semi-field studies this hypothesis was tested for the aphid Rhopalosiphum maidis (Fitch) (Rhynchota, Sternorrhyncha, Aphididae).In a Y-tube olfactometer significantly more aphids chose the odour of healthy, undamaged maize seedlings when tested against clean air or plants treated with regurgitant. Clean air was chosen more often when tested next to the odour of treated plants. This apparently repellent effect of the odour of treated plants was significant for winged aphids, but not for the wingless aphids.In field experiments aphids were released in the centre of circles of eight potted maize plants. Four plants in each circle were damaged and treated with caterpillar regurgitant while the other plants were left unharmed. At different intervals after aphid release, the number of aphids was counted on each plant. Significantly fewer winged and wingless aphids were found back on treated plants than on healthy plants.We suggest that herbivores may be repelled by the odours because they could indicate that: 1) the plant has initiated the production of toxic compounds; 2) potential competitors are present on the plant; 3) the plant is attractive to parasitoids and predators. Aphids may be particularly sensitive to induced maize volatiles because one of the major compounds emitted by the plant is (E)--farnesene, which is a common alarm pheromone for aphids. Collections and analyses of the odours emitted by crushed R. maidis confirmed that it too emits (E)--farnesene when stressed. The results are discussed in context of plant defence strategies and their possible exploitation for the control of pest insects.     

How aphids find their host plants,and how they don't

There is a considerable interest in trying to understand how aphids find their host plants because they are a major cause of economic losses in agricultural and horticultural production systems. Indeed, the specific behavioural sequences during host finding by aphids are one of the main reasons for their prominent role as vectors of plant pathogenic viruses. This paper reviews the visual and olfactory stimuli involved in host‐finding behaviour of aphids, both basic and applied aspects are covered. Although controlling aphids by manipulation of visual and olfactory stimuli involved in host finding and host selection can be highly successful, as shown by research, most of these measures can still be further optimised and adoption in practice is currently limited. Research therefore needs to address some critical open questions, including (a) the effects of visual contrasts on aphid behaviour; (b) the specific responses of aphids to ultraviolet (UV) light during different stages in host finding; (c) the quantification of behavioural sequences in the field and (d) the response of aphid behaviour to plant diversity at varying spatial scales; further, (e) a much more comprehensive coverage of aphid taxa and aphid ecological groups is needed in host‐finding related research to uncover ecological principles underlying this critical behaviour.     

Soybean Aphid Response to their Alarm Pheromone E-ß-Farnesene (EBF)

When attacked by natural enemies some insect pests, including many aphid species, alert neighboring conspecifics with alarm pheromones. Cornicle secretions with pheromones benefit the attacked aphid but are costly to produce, while alarm pheromone benefits probably fall largely on alerted conspecifics. Given these variable benefits, the likelihood of a secretion may change depending on aphid density. Thus, we first hypothesized that the common alarm pheromone in aphids, E-ß-farnesene (EBF), was present in soybean aphid (Aphis glycines Matsumura) cornicle secretions and would elicit an alarm response in aphids exposed to it. Second, since aphids other than the secretor also benefit from cornicle secretions, we hypothesized that the likelihood of secretion would increase concurrently with the density of neighboring clonal conspecifics. Third, because alarm reaction behavior (e.g. feeding cessation) is probably costly, we hypothesized that alarm reaction behavior would decrease as conspecific density (i.e. alternative prey for an attacking natural enemy) increased. We found that soybean aphids 1) produce cornicle secretions using EBF as an alarm pheromone, 2) are less likely to release cornicle secretions when alone than in a small group (~10 individuals), but that the rate of secretion does not increase further with additional conspecific density, and 3) also exhibit alarm reaction behavior in response to cornicle secretions independent of aphid density. We show that soybean aphids can use their cornicle secretions to warn their neighbors of probable attack by natural enemies, but that both secretion and alarm reaction behavior does not change as density of nearby conspecifics rises above a few individuals.     

Cultivar‐specific plant odour preferences of a generalist aphid parasitoid Aphidius colemani and a possible mechanism for maternal priming of resistance to toxic plant chemistry

Aphidius colemani Viereck, emerging from Myzus persicae (Sulzer) mummies on the Brussels sprout cultivar ‘Bedford Winter Harvest’ (BWH), responds positively in the olfactometer to the odour of that cultivar in comparison with air. Responses to the odours of other sprout cultivars, cabbage and broad bean could be explained by the humidity from plant leaves. In a choice between BWH and other sprout cultivars, the BWH odour is preferred, or that of cv. ‘Red Delicious’ (RD) if the parasitoids are reared on RD. This confirms previous work showing that the secondary chemistry of a cultivar is learnt from the mummy cuticle during emergence. Adults emerging from pupae excised from the mummy show a similar but less pronounced preference. Parasitoids developing in aphids on an artificial diet do not discriminate between the odours of BWH and RD, unless allowed contact with a mummy from the same cultivar that the mother develops on. This suggests a cultivar‐specific maternal cue. This cue is speculated to consist of a small amount of the secondary chemistry (probably glucosinolates in the present study) that are left in or on the egg at oviposition, which subsequently induces enzymes that detoxify plant‐derived toxins in the aphid host. Indeed, when parasitoids emerging from diet‐reared aphids are released on aphid‐infested sprout plants, fewer mummies are produced than by parasitoids emerging from mummies of plant‐reared aphids or from excised pupae. Only parasitoids that emerge from mummies of plant‐reared aphids prefer the cultivar of origin as shown by the number of mummified hosts.     

Function of the siphunculi in aphids with particular reference to the sycamore aphid, Drepanosiphum platanoides

Sycamore aphids with occluded siphunculi survive, give birth to as many offspring and maintain their weight as well as aphids with normal siphunculi and it is therefore unlikely that siphunculi have an excretory function. Blocking the siphunculi of sycamore aphids does not affect the way they space out. Siphunculi are used in defence against predators most effectively when the aphid and predator are similar in size.The smell of siphuncular exudate causes aphids like Myzus persicae to scatter but in the sycamore aphid the smell has to be accompanied by the sight or vibration of a struggling aphid to induce an alarm response. Prodding the abdomen and pinching the legs of a sycamore aphid induces it to produce siphuncular exudate.     

Influence of Experience on the Response of Bathyplectes curculionis (Hymenoptera: Ichneumonidae), a Nonaphidophagous Parasitoid, to Aphid Odor

Bathyplectes curculionis (Thomson) is an introduced natural enemy of the alfalfa weevil in North America. The wasp requires carbohydrate foods as an adult. Adult wasps have increased longevity and fecundity when provided access to pea aphid, Acyrthosiphon pisum (Harris), honeydew in the laboratory, and adults respond positively to the presence of pea aphids in alfalfa fields. However, it is unknown how these wasps find aphid honeydew in the field. In a series of Y-tube olfactometer experiments, we evaluated the response of naïve and experienced adult female B. curculionis to odors from pea aphids, alfalfa, and pea aphids on alfalfa. Naïve adult females did not respond positively to pea aphid odor even when hungry. But adult females were able to learn aphid odor, and the mechanism of learning appears to be associative rather than by sensitization. Naïve females also showed no preference for alfalfa odor but learned alfalfa odor through sensitization. The wasps did not distinguish between alfalfa with aphids and alfalfa without aphids, even after exposure to aphids or alfalfa with aphids. However, they preferred pea aphid odor to alfalfa odor after a feeding experience in the presence of pea aphid odors. But after exposure to mixed odors of aphids and alfalfa while feeding, B. curculionis females preferred the odor of alfalfa to the odor of pea aphids. These results suggest that alfalfa odors mask or override aphid odors when aphids are associated with alfalfa (as happens naturally), thus interfering with the wasp's ability to respond to learned aphid odors. Therefore, although the wasps are capable of learning to find pea aphids and their honeydew in a simplified laboratory setting, it appears unlikely that they do so in the field.     

The importance of antennae for pea aphid wing induction in the presence of natural enemies

The pea aphid Acyrthosiphon pisum Harris has been shown to produce an increasing proportion of winged morphs among its offspring when exposed to natural enemies, in particular hoverfly larvae, lacewing larvae, adult and larval ladybirds and aphidiid parasitoids. While these results suggest that wing induction in the presence of predators and parasitoids is a general response of the pea aphid, the cues and mechanisms underlying this response are still unclear. Tactile stimuli and the perception of chemical signals as well as visual signals are candidates for suitable cues in the presence of natural enemies. In this paper the hypothesis that the aphids' antennae are crucial for the wing induction in the presence of natural enemies is tested. Antennae of pea aphids were ablated and morph production was scored when aphids were reared either in the presence or the absence of predatory lacewing larvae over a six-day period. Ablation of antennae resulted in a drastic drop in the proportion of winged morphs among the offspring, both in the presence and the absence of a predator whereas predator presence increased wing induction in aphids with intact antennae, as reported in previous experiments. The results show that antennae are necessary for wing induction in the presence of natural enemies. Critical re-examination of early work on the importance of aphid antennae and tactile stimuli for wing induction suggests that a combination of tactile and chemical cues is likely to be involved not only in predator-induced wing formation but also for wing induction in response to factors such as crowding in the aphid colony.     

Why do ants shift their foraging from extrafloral nectar to aphid honeydew?

When aphids parasitize plants with extrafloral nectaries (EFNs) and aphid colony size is small, ants frequently use EFNs but hardly tend aphids. However, as the aphid colony size increases, ants stop using EFNs and strengthen their associations with aphids. Although the shift in ant behavior is important for determining the dynamics of the ant–plant–aphid interaction, it is not known why this shift occurs. Here, we test two hypotheses to explain the mechanism responsible for this behavioral shift: (1) Extrafloral nectar secretion changes in response to aphid herbivory, or (2) plants do not change extrafloral nectar secretion, but the total reward to ants from aphids will exceed that from EFNs above a certain aphid colony size. To judge which mechanism is plausible, we investigated secretion patterns of extrafloral nectar produced by plants with and without aphids, compared the amount of sugar supplied by EFNs and aphids, and examined whether extrafloral nectar or honeydew was more attractive to ants. Our results show that there was no inducible extrafloral secretion in response to aphid herbivory, but the sugar concentration in extrafloral nectar was higher than in honeydew, and more ant workers were attracted to an artificial extrafloral nectar solution than to an artificial aphid honeydew solution. These results indicate that extrafloral nectar is a more attractive reward than aphid honeydew per unit volume. However, even an aphid colony containing only two individuals can supply a greater reward to ants than EFNs. This suggests that the ant behavioral shift may be explained by the second hypothesis.     

Effect of synthetic aphid alarm pheromone (E) -beta-farnesene on development and reproduction of Aphis gossypii (Homoptera: Aphididae)

The synthetic aphid alarm pheromone (E)-beta-farnesene (EBF) is released by aphids in response to predation or other disturbances that occur in the colony. This is presumed to benefit the population by allowing increased survival of related individuals taking successful evasive action after perception of the pheromone. The effect of pheromone perception by aphids in the absence of real threats was investigated to determine the baseline effect of this communication on aphid survival, development, and fecundity in the laboratory. All four nymphal stages of cotton aphid, Aphis gossypii Glover (Homoptera: Aphididae), were stimulated with EBF. No significant difference in survival rates was observed in the aphids stimulated with EBF compared with the untreated control. Developmental times of the aphids were significantly prolonged in first and third instars when they were stimulated with EBF. Significantly lower fecundity and lighter weight of adult aphids were observed in aphids stimulated with EBF at as first instars compared with untreated controls and other instars. Results indicate that exposure of the first instar of A. gossipii to the synthetic alarm pheromone adversely affects subsequent development and fecundity of the population. This reduces aphid fitness that must be compensated by increased survival from predation for the pheromone to confer a selective advantage to the species.     

Collective Defense of Aphis nerii and Uroleucon hypochoeridis (Homoptera,Aphididae) against Natural Enemies

The prevalent way aphids accomplish colony defense against natural enemies is a mutualistic relationship with ants or the occurrence of a specialised soldier caste typcial for eusocial aphids, or even both. Despite a group-living life style of those aphid species lacking these defense lines, communal defense against natural predators has not yet been observed there. Individuals of Aphis nerii (Oleander aphid) and Uroleucon hypochoeridis, an aphid species feeding on Hypochoeris radicata (hairy cat''s ear), show a behavioral response to visual stimulation in the form of spinning or twitching, which is often accompanied by coordinated kicks executed with hind legs. Interestingly, this behaviour is highly synchronized among members of a colony and repetitive visual stimulation caused strong habituation. Observations of natural aphid colonies revealed that a collective twitching and kicking response (CTKR) was frequently evoked during oviposition attempts of the parasitoid wasp Aphidius colemani and during attacks of aphidophagous larvae. CTKR effectively interrupted oviposition attempts of this parasitoid wasp and even repelled this parasitoid from colonies after evoking consecutive CTKRs. In contrast, solitary feeding A. nerii individuals were not able to successfully repel this parasitoid wasp. In addition, CTKR was also evoked through gentle substrate vibrations. Laser vibrometry of the substrate revealed twitching-associated vibrations that form a train of sharp acceleration peaks in the course of a CTKR. This suggests that visual signals in combination with twitching-related substrate vibrations may play an important role in synchronising defense among members of a colony. In both aphid species collective defense in encounters with different natural enemies was executed in a stereotypical way and was similar to CTKR evoked through visual stimulation. This cooperative defense behavior provides an example of a surprising sociality that can be found in some aphid species that are not expected to be social at all.     

Orientation by polarized light in the crayfish dorsal light reflex: behavioral and neurophysiological studies

In decapod crustaceans, the dorsal light reflex rotates the eyestalk so that the dorsal retina faces the brightest segment of dorsal visual space. Stepwise displacements of white stripes elicit eyestalk rotations in the same direction as that of the stripe. Conversely, stepwise displacements of black stripes on a white background elicit eyestalk rotations in the opposite direction as that of the stripe. The reversal of the response with contrast inversion distinguishes the dorsal light reflex from an optokinetic reflex. When the visual scene is composed of polarized light, segmented by variations in e-vector orientation, displacement of segments containing near vertical e-vectors elicit responses similar to those elicited by a white stripe. Displacement of polarized stripes containing near horizontal e-vectors elicit eyestalk rotations similar to those elicited by a black stripe. The results are consistent with the use of polarized light in orientation. The stimulus conditions described above were also applied to visual interneurons (sustaining fibers) and oculomotor neurons and the results were generally in accord with the behavior. In the neural studies, it was possible to show that responses to polarized stripe displacements are predictable from the receptive field location and the neuron’s polarization tuning function. John P. Schroeter deceased on September 14, 2006.     

Specificity of sex pheromones, the role of host plant odour in the olfactory attraction of males, and mate recognition in the aphid Cryptomyzus

Abstract. Choice tests in an olfactometer showed that males of the aphid Cryptomyzus galeopsidis spent more time in the odour of conspecific females than of a sibling species or a more distantly related Cryptomyzus species, which all co-occur on red currant. Analysis of the pheromone-emissions of females showed the presence of a nepetalactol and a nepetalactone, two known aphid sex pheromone components. However, no interspecific difference in the ratio of the components ( c. 30:1) was found, and this ratio did not change as the females aged. Males were only slightly attracted by a synthetic 30:1 mixture of these two components, and in a choice test preferreď the odour of conspecific females. The sex pheromone of Cryptomyzus spp. must thus consist of more than two components, the first time this has been reported for aphids. Host plant odour did not attract males or enhance the activity of the pheromone.     

The spatial dynamics of crop and ground active predatory arthropods and their aphid prey in winter wheat

The distribution of aphid predators within arable fields has been previously examined using pitfall traps. With this technique predominantly larger invertebrate species are captured, especially Carabidae, but the technique provides no estimate of density unless mark-recapture is used. However, many other numerically important aphid predators occur in arable fields and relatively little is known about their distribution patterns nor whether they exhibit a density-dependent response to patches of cereal aphids. Identification of the most effective predators can allow management practices to be developed accordingly. In this study, the distribution of cereal aphids and their predators was examined by suction sampling within a field of winter wheat in Devon, UK, along with visual estimates of weed patchiness. Sampling was conducted on four occasions in 1999 across a grid of 128 sample locations. The distribution of 11 predatory taxa from the Carabidae, Staphylinidae and Linyphiidae was examined. Additionally, the total number of aphid predators and a predation index were used in these analyses. Carabid adults and larvae, along with staphylinid larvae showed the strongest aggregation into patches and the most temporal stability in their distribution. Other taxa had more ephemeral distributions as did the cereal aphids. The distribution of carabid larvae was disassociated from the distribution of cereal aphids for the first two sampling occasions indicating biocontrol was occurring. Other predatory groups showed both association and disassociation. Carabid larvae, Bathyphantes and total numbers of Linyphiidae showed a strong correlation with weed cover for two of the sample dates. Cereal aphids were disassociated from weed cover on three sampling occasions.     

Hoverfly oviposition response to aphids in broccoli fields

The oviposition response of predacious hoverflies (Diptera: Syrphidae) to Brevicoryne brassicae L. and Myzus persicae (Sulzer) (Homoptera: Aphididae) in commercial broccoli, Brassica oleracea var. italica L., Plenck (Brassicaceae), fields was investigated at two sites over the course of a growing season. The hoverfly oviposition responses to these aphid species on different parts of the broccoli plant canopy were also examined. There were no hoverfly eggs on broccoli plants without aphids, egg numbers were very low on plants with fewer than 50 aphids, and no peak in oviposition relative to aphid numbers was observed. Within individual plants that were colonized by aphids, there was some oviposition on individual leaves without aphids, and no hoverfly eggs were seen on leaves that had more than 400 aphids. Leaves in the broccoli plant canopy, and the datasets associated with them, were divided into three sections vertically, ‘upper’, ‘middle’, and ‘lower’. Brevicoryne brassicae was more abundant in the upper and middle canopy sections, while M. persicae was found mostly in the lower section. The rate of hoverfly oviposition per aphid was higher in the upper section than in the two other sections. Modeling of the oviposition response using logistic regression showed that the presence of hoverfly eggs was positively correlated with numbers of each aphid species and sampling date.