The escape response of pea aphids to foliar-foraging predators: factors affecting dropping behaviour

1. The effects of predator species, aphid density, aphid age, diel period, and habitat complexity on the dropping behaviour of the pea aphid Acyrthosiphon pisum were assessed in a series of laboratory and field-cage experiments.
2. The presence of foliar-foraging predators significantly increased the proportion of aphids that dropped from alfalfa plants. In the absence of predators, less than 7% of the aphids dropped. Dropping more than doubled (14%) when one of three hemipteran predators , N. americoferus, G. punctipes or O. insidiosus , was present. Nearly 60% of the aphids dropped when the ladybird beetle, Coccinella septempunctata , was present.
3. Adult aphids showed a significantly higher propensity to drop than immature aphids, regardless of the presence or absence of predators. Aphid density had no effect on dropping behaviour.
4. Neither diel period nor habitat complexity had an effect on aphid dropping behaviour. Aphids were significantly more likely to drop in the presence of predators during either the day or night and from either early or late regrowth alfalfa.
5. A review of the factors affecting dropping behaviour, including those elucidated in this study, indicates that the propensity to drop from a plant is influenced by three factors: the risk of predation on the plant, the quality of the resource to be abandoned, and the risk of mortality in the new microhabitat.     

Non‐consumptive effects of a natural enemy on a non‐prey herbivore population

1. Predator–prey interactions have traditionally focused on the consumptive effects that predators have on prey. However, predators can also reduce the abundance of prey through behaviourally‐mediated non‐consumptive effects. For example, pea aphids (Acyrthosiphon pisum Harris) drop from their host plants in response to the risk of attack, reducing population sizes as a consequence of lost feeding opportunities. 2. The objective of the present study was to determine whether the non‐consumptive effects of predators could extend to non‐prey herbivore populations as a result of non‐lethal incidental interactions between herbivores and foraging natural enemies. 3. Polyculture habitats consisting of green peach aphids (Myzus persicae Sulzer) feeding on collards and pea aphids feeding on fava beans were established in greenhouse cages. Aphidius colemani Viereck, a generalist parasitoid that attacks green peach aphids but not pea aphids, was released into half of the cages and the abundance of the non‐host pea aphid was assessed. 4. Parasitoids reduced the population growth of the non‐host pea aphid by increasing the frequency of defensive drops; but this effect was dependent on the presence of green peach aphids. 5. Parasitoids probably elicited the pea aphid dropping behaviour through physical contact with pea aphids while foraging for green peach aphids. It is unlikely that pea aphids were responding to volatile alarm chemicals emitted by green peach aphids in the presence of the parasitoid. 6. In conclusion, the escape response of the pea aphid provided the opportunity for a parasitoid to have non‐target effects on an herbivore with which it did not engage in a trophic interaction. The implication is that natural enemies with narrow diet breadths have the potential to influence the abundance of a broad range of prey and non‐prey species via non‐consumptive effects.     

Alarm pheromone mediates production of winged dispersal morphs in aphids

The aphid alarm pheromone ( E )- β -farnesene (EBF) is the major example of defence communication in the insect world. Released when aphids are attacked by predators such as ladybirds or lacewing larvae, aphid alarm pheromone causes behavioural reactions such as walking or dropping off the host plant. In this paper, we show that the exposure to alarm pheromone also induces aphids to give birth to winged dispersal morphs that leave their host plants. We first demonstrate that the alarm pheromone is the only volatile compound emitted from aphid colonies under predator attack and that emission is proportional to predator activity. We then show that artificial alarm pheromone induces groups of aphids but not single individuals to produce a higher proportion of winged morphs among their offspring. Furthermore, aphids react more strongly to the frequency of pheromone release than the amount of pheromone delivered. We suggest that EBF leads to a 'pseudo crowding' effect whereby alarm pheromone perception causes increased walking behaviour in aphids resulting in an increase in the number of physical contacts between individuals, similar to what happens when aphids are crowded. As many plants also produce EBF, our finding suggests that aphids could be manipulated by plants into leaving their hosts, but they also show that the context-dependence of EBF-induced wing formation may hinder such an exploitation of intraspecific signalling by plants.     

Dropping of pea aphids from feeding site: a consequence of parasitism by the wasp, Monoctonus paulensis

We examined the dropping behaviour of the pea aphid, Acyrthosiphon pisum (Harris), feeding on broad-bean plants in the laboratory. Aphid responses to foraging and oviposition by females of Monoctonus paulensis (Ashmead) were instar-specific and included kicking with the hind legs, walking away and dropping from the feeding site. Fourth nymphal instars were most likely to drop, followed by second, third, and first instars, in that order. Compared with first instars, the odds that a fourth-instar aphid will drop were 6-times higher independent of the stimulus, and 16-times higher after parasitoid attack. Dropping from the feeding site increases an aphid's mortality risk. If parasitoid offspring are more likely to survive in small pea aphids, it may be adaptive for M. paulensis to choose smaller hosts, regardless of possible fitness gains due to increased body size from development in larger aphids.     

Influence of aphid size,age and behaviour on host choice by the parasitoid wasp Ephedrus californicus: a test of host-size models

Summary When host quality varies, parasitoid wasps are expected to oviposit selectively in high-quality hosts. We tested the assumption underlying host-size models that, for solitary species of wasps, quality is based on host size. Using Ephedrus californicus, a solitary endoparasitoid of the pea aphid, we evaluated the influence of aphid size (= mass), age and defensive behaviours on host selection. Experienced parasitoid females were given a choice among three classes of 5-day-old apterous nymphs: small aphids that had been starved daily for 4 h (S4) and 6 h (S6) respectively, and large aphids permitted to feed (F) normally. Wasps attacked more, and laid more eggs in, small than large aphids (S6>S4>F). This rank-order for attack did not change when females could choose among aphids of the same size that differed in age; however, wasps oviposited in all attacked aphids with equal probability. Host size did not influence parasitoid attack rates when aphids were anaesthetized so that they could not escape or defend themselves. As predicted by host-size models, wasp size increased with host size (F>S4; S6), but large wasps required longer to complete development than their smaller counterparts (S4E. californicus reflects a trade-off between maximization of fitness gains per egg and the economics of search-time allocation. Because large aphids are more likely to escape parasitization, a wasp must balance her potential gain in fitness by ovipositinng in a high-quality (large) aphid against her potential cost in terms of lost opportunity time if the attack fails.     

Cucurbit aphid‐borne yellows virus (CABYV) modifies the alighting,settling and probing behaviour of its vector Aphis gossypii favouring its own spread

Plant pathogens are able to influence the behaviour and fitness of their vectors in such a way that changes in plant–pathogen–vector interactions can affect their transmission. Such influence can be direct or indirect, depending on whether it is mediated by the presence of the pathogen in the vector's body or by host changes as a consequence of pathogen infection. We report the effect that the persistently aphid‐transmitted Cucurbit aphid‐borne yellows virus (CABYV, Polerovirus) can induce on the alighting, settling and probing behaviour activities of its vector, the cotton aphid Aphis gossypii. Only minor direct changes on aphid feeding behaviour were observed when viruliferous aphids fed on non‐infected plants. However, the feeding behaviour of non‐viruliferous aphids was very different on CABYV‐infected than on non‐infected plants. Non‐viruliferous aphids spent longer time feeding from the phloem in CABYV‐infected plants compared to non‐infected plants, suggesting that CABYV indirectly manipulates aphid feeding behaviour through its shared host plant in order to favour viral acquisition. Viruliferous aphids showed a clear preference for non‐infected over CABYV‐infected plants at short and long time, while such behaviour was not observed for non‐viruliferous aphids. Overall, our results indicate that CABYV induces changes in its host plant that modifies aphid feeding behaviour in a way that virus acquisition from infected plants is enhanced. Once the aphids become viruliferous they prefer to settle on healthy plants, leading to optimise the transmission and spread of this phloem‐limited virus.     

Patterns of host selection by four species of aphidiid (Hymenoptera) parasitoids: influence of host switching

Abstract.

• 1 We tested switching behaviour in four species of aphidiid parasitoids, using a two-aphid experimental system consisting of second-instar nymphs of pea aphid (Acyrthosiphon pisum (Harris)) and alfalfa aphid (Macrosiphum creelii Davis) feeding on broad beans in the laboratory.
• 2 Aphidius ervi Haliday, A.pisivorus Smith, A.smithi Sharma & Subba Rao, and Pram pequodorum Viereck showed an innate preference for pea aphid when both host species were provided in equal numbers.
• 3 Wasps encountered both aphid species equally but differed in their acceptance of alfalfa aphid. Females of A.pisivorus and P.pequodorum accepted alfalfa aphids when few pea aphids were available, but A. smithi always concentrated attacks on pea aphid. Aphidius ervi super-parasitized an increasing proportion of pea aphids as their availability declined.
• 4 Switching to the alfalfa aphid occurred in A.ervi and P.pequodorum (but not in A.pisivorus and A.smithi) under the condition of a 1:3 ratio of pea aphids:alfalfa aphids. Wasps did not switch when more pea aphids than alfalfa aphids were provided (3:1 ratio).
• 5 Alfalfa aphids were more likely than pea aphids to escape from parasitoid attack.
• 6 Switching to the most abundant host may not be adaptive in these four species of aphid parasitoids. A foraging wasp incurs a potentially higher cost in lost opportunity time when attacking (and failing to oviposit in) alfalfa aphids. In addition, alfalfa aphids may have lower host quality than pea aphids, a difference that could influence offspring fitness.

     

How aphid alarm pheromone can control aphids: a review

Aphids are the major pests of arable crops, mostly in temperate regions. They are monophagous as well as polyphagous. They inflict damage in brassica, potato, cotton, vegetable and fruit crops. They damage their host plant directly by feeding upon their phloem sap, or indirectly by transmitting pathogens to them. Their life cycle can be autoecious as well as heteroecious. Aphids use semiochemicals for various purposes, in gathering information from their environment and for communication among themselves. They protect themselves from predators and parasitoids by escape response which is arbitrated by use of alarm pheromone signalling. When alarm pheromone, (E)-ß-farnesene, is released, nearby aphids exhibit a variety of behaviours like moving away, running, dropping off the plant and even attacking the predator. Previous studies of integrated pest management strategies have been aimed at the usage of alarm pheromone. However, scientists require complete knowledge of aphid ecology as well as aphid interaction with its natural enemies to establish efficient and viable biological control. This review presents analysis of the existing aphid pest management methodologies and effectiveness of alarm pheromone on aphids and their natural enemies.     

Cues of Predation Risk Induce Instar‐ and Genotype‐Specific Changes in Pea Aphid Colony Spatial Structure

Deploying collective antipredator behaviors during periods of increased predation risk is a major determinant of individual fitness for most animal groups. Pea aphids, Acyrthosiphon pisum, which live in aggregations of genetically identical individuals produced via asexual reproduction warn nearby conspecifics of pending attack by secreting a volatile alarm pheromone. This alarm pheromone allows clone‐mates to evade predation by walking away or dropping off the host plant. Here, we test how a single alarm pheromone emission influences colony structure and defensive behavior in this species. Relative to control colonies, groups exposed to alarm pheromone exhibited pronounced escape behavior where many individuals relocated to adjacent leaves on the host plant. Alarm pheromone reception, however, also had subtle instar‐specific effects: The proportion of 1st instars feeding nearest the leaf petiole decreased as these individuals moved to adjacent leaves, while the proportion of 2nd–3rd instars feeding nearest the leaf petiole remained constant. Fourth instars also dispersed to neighboring leaves after pheromone exposure. Lastly, alarm pheromone reception caused maternal aphids to alter their preferred feeding sites in a genotype‐specific manner: Maternal aphids of the green genotype fed further from the petiole, while maternal aphids of the pink genotype fed closer to the petiole. Together, our results suggest that aphid colony responses to alarm pheromone constitute a diversity of nuanced instar‐ and genotype‐specific effects. These behavioral responses can dramatically change the spatial organization of colonies and their collective defensive behavior.     

Differences in escape behavior between pea aphid biotypes reflect their host plants’ palatability to mammalian herbivores

Phytophagous insects have evolved traits that help them avoid predation risks, traits that may be affected by characteristics of the host plant. Since most phytophagous insects have narrow host ranges, we expect differences in risk avoidance between plant-specialized populations of several closely related insect lineages. To test this hypothesis, we used the pea aphid (Acyrthosiphon pisum), which forms a complex of about 15 biotypes, each adapted to one or a few species of legume plants (Fabaceae). We examined the differences in defensive behaviors of 38 clones from 13 distinct plant-specialized biotypes of pea aphids. We exposed mature aphids to simulated breath of a mammalian herbivore, a cue that causes part of the aphids in a colony to immediately drop off the plant to avoid incidental ingestion during mammal feeding. Dropping tendency varied substantially between biotypes (15–93% average rates). Dropping rates of a certain biotype of aphid reflected their host’s palatability to mammalian herbivores, with ∼80–90% rates in fodder and pasture plants and ∼15–40% dropping in inedible plants. The dropping tendency showed no correlation with walking ability (tarsal & body length), nor with the tendency to escape in response to the alarm pheromone released by conspecifics in response to arthropod enemies. The specialization on a specific host plant brings with it particular selective pressures, and it seems that the palatability of the plants to mammals promotes behavioral divergence between biotypes, reinforcing diversification through ecological divergence.     

Antipredator responses of aphids to parasitoids change as a function of aphid physiological state

Under predation risk, prey may prioritize antipredator behaviours and sacrifice feeding. However, energetically constrained animals may choose to sacrifice or change antipredator responses and accept relatively greater risk in order to secure food. In this last case, the antipredator tactics chosen must balance safety and feeding in such a way that costs are minimized and benefits maximized. We studied the antipredator behaviour of pea aphid, Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) subjected to different periods of food deprivation, against the parasitoid Aphidius ervi (Hymenoptera: Braconidae). As the energetic internal stress of aphids increased, the predominant antipredator response changed from walking away and dropping to kicking behaviour, and parasitization avoidance decreased. Parasitoids did not show preference between food-deprived and nonfood-deprived aphids. Dropping and walking away reduced parasitization from 50 to 33%. These results support the hypothesis that the antipredator behaviour of an aphid changes as a function of internal stress. By performing less costly behaviour such as kicking under energetically constrained conditions, aphids seem to minimize their probability of energy shortfall. Given that aphid antipredator behaviour is a function of nutritional state, its occurrence under natural conditions may match host quality spatial distribution. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Alarm pheromone emission by pea aphid, Acyrthosiphon pisum, clones under predation by lacewing larvae

Genetic variation in anti-predator traits has been shown for a variety of species. Aphid alarm pheromone, ( E )-β-farnesene, is released by attacked aphids and causes a variety of behavioral defense reactions in the signal receivers. In pea aphids, Acyrthosiphon pisum Harris (Homoptera: Aphididae), ( E )-β-farnesene mediates the production of winged offspring in the presence of natural enemies. While variation in the propensity for pea aphids to produce winged offspring is well-documented, little quantitative information is available about clonal differences in ( E )-β-farnesene emission or the amount of alarm pheromone released in aphid colonies. We tested the wing induction response of four clones when attacked by a predatory lacewing larva, Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae), and found that three of the four clones increased the proportion of winged offspring under predator attack. We then investigated the emission of aphid alarm pheromone of these clones of pea aphid under attack. Alarm pheromone emission in aphid colonies of initially 25 adults varied from 81.2 to 10 851.0 ng per aphid colony over 24 h. There were no differences between clones in total emission or in emission per consumption event. These results show that there is substantial variability in alarm pheromone emission within clones and that the propensity to produce winged offspring in some clones is not a simple function of the propensity of alarm pheromone production in these clones.     

Standing on the shoulders of giants: young aphids piggyback on adults when searching for a host plant

Background

Upon the detection of imminent peril, pea aphids (Acyrthosiphon pisum) often drop off their host plant. Dropping in response to insect enemies is intermittent in nature, but when a mammalian herbivore feeds on their host plant, a large mixed-age group of aphids usually drops off the plant at once. Aphids that reach the ground are confronted with new, hostile environmental conditions and must therefore quickly walk toward a suitable host plant. The longer it takes an aphid to reach a host plant, the more it is exposed to the risks of starvation, desiccation and predation.

Results

We found that young nymphs, which have limited mobility and high mortality on the ground, quickly climb on conspecific (not necessarily parental) adults and cling to them before the latter start walking in search of a plant. This “riding” behavior is likely to be adaptive for the nymphs, for it shortens their journey and the time they spend off a host plant. Adults however, seem to be irritated by the riding nymphs, as they often actively try to remove them.

Conclusions

After dropping from the host plant, young aphid nymphs travel at least part of the way back to a plant on the backs of adults. For the riding behavior to take place, nymphs need to successfully find adults and withstand removal attempts.

     

Do aphids infected with entomopathogenic fungi continue to produce and respond to alarm pheromone?

The response of pea aphids, Acyrthosiphon pisum, to aphid alarm pheromone was not modified by infection with Beauveria bassiana. Approximately 50% of uninfected and infected aphids responded to synthetic alarm pheromone. The simulated attack of aphids infected with B. bassiana did not elicit a response in uninfected aphids. Preliminary air entrainment experiments of both uninfected aphids and aphids at different stages of B. bassiana (generalist pathogen) or P. neoaphidis (obligate pathogen of aphids) demonstrated that B. bassiana infected aphids produced less alarm pheromone than uninfected aphids and, conversely, P. neoaphidis infected aphids produced more alarm pheromone than uninfected aphids. These results are discussed with particular emphasis on the different life history strategies of these two pathogens. We hypothesise that the obligate, specialist pathogen, P. neoaphidis, is under greater selection pressure to increase pathogen transmission and survival resulting in modified host behaviour, than the generalist pathogen, B. bassiana.     

Is the response of aphids to alarm pheromone stable?

Aphid taxa are characterized by a number of biological features, such as their feeding behaviour and host selection, which it is generally accepted are affected by keeping them for several generations under standard conditions in a laboratory. Analyses of three strains of the green pea aphid, Acyrthosiphon pisum (Harris, 1776), reared in culture for long periods, indicate that other characters are also affected. For example, the response of these aphids to alarm pheromone is dramatically reduced. This raises an interesting question regarding the mechanism by which it occurs and has consequences when aphids from laboratory cultures are used for studies in ecology and applied biology and especially the long‐term effectiveness of crop plants genetically engineered to produce EBF as a means of controlling aphids.     

Rearing history affects behaviour and performance of two virulent Nasonovia ribisnigri populations on two lettuce cultivars

Many aphid species have become virulent to host‐plant resistance, which limits the sustainability of insect resistance breeding. However, when this adaptation to resistant plants is associated with fitness costs for the aphids, virulence can be lost in the absence of resistant plants. For two populations of the lettuce aphid, Nasonovia ribisnigri (Mosely) (Hemiptera: Aphididae), we evaluated whether virulence to Nr‐gene‐based resistance was lost on a susceptible lettuce, Lactuca sativa L. (Asteraceae), and assessed possible costs of virulence. The feeding behaviour and performance of these aphids, reared and tested on susceptible and resistant lettuce, were investigated. The rearing plant affected feeding behaviour and performance of the aphids. Temporary reduction and long‐term loss of virulence were found. The total duration of phloem intake was shorter after being reared on susceptible lettuce and tested on resistant lettuce. In addition, one population had a lower survival on resistant lettuce after being reared on susceptible lettuce. There were also indications of fitness costs of the virulence in both populations.     

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.     

Searching behaviour and mate recognition by males of the two-spot ladybird beetle, Adalia bipunctata

Abstract. 1. Adult males of the two-spot ladybird beetle, Adalia bipunctata , did not show a functional response to increase in aphid abundance and consumed markedly fewer aphids than do the females.
2. At high densities of prey, females spent more time in area-restricted search than when prey was scarce. Males were always less active than females and they did not respond to an increase in prey abundance by a change in searching behaviour.
3. After a brief encounter with a female, a male showed area-restricted searching behaviour. This behaviour occurred in response to encountering a female's elytra and in particular to a chloroform-soluble component (sex pheromone) present on or in the elytra.
4. Males needed to encounter a female in order to respond to her presence, which indicated the pheromone is a contact pheromone.
5. The searching behaviour of males appeared to be mainly directed towards locating females; that of females towards locating aphids. This difference between the sexes should be taken into account when quantifying the predatory response of ladybirds to aphid abundance in the field.     

Plant water stress intensity mediates aphid host choice and feeding behaviour

1. The effects of drought-induced changes in plant quality on aphid performance and population growth is well-studied. The response of aphid behaviour to plant water limitation has received less attention. Water limitation may affect host-plant colonization by altering the attractiveness of plants. Additionally, plant water limitation may inhibit feeding site establishment and phloem ingestion.
2. Our goal was to examine bird cherry-oat aphid (Rhopalosiphum padi L.) host selection and feeding behaviour under water limitation. We assessed aphid response to well-watered, mildly-stressed, and highly-stressed wheat (Triticum aestivum L.) by evaluating (i) host-plant selection through two-choice assays, (ii) feeding behaviour using the electrical penetration graph technique, and (iii) phloem ingestion by quantifying honeydew production.
3. Aphids were less likely to select highly stressed plants than a mildly stressed or well-watered alternative. Aphids did not distinguish between mildly stressed and well-watered plants. Aphid feeding behaviours, including duration of phloem ingestion, were not affected by water availability. However, honeydew production was reduced under both levels of water limitation. These results suggest that the volume of phloem ingested by aphids per unit time declined on stressed plants. The combination of lower colonization and diminished access to food on stressed plants may lead to a reduction in aphid abundance, independent of the direct effects of nutrition on individual aphid performance.
4. This study highlights the potential contribution of herbivore behaviour to documented changes in aphid abundance on stressed plants and underscores the important role of plant water stress intensity in mediating plant-herbivore interactions.

     

Emission of alarm pheromone by non-preyed aphid colonies

The sesquiterpene (E)-β-farnesene (Eβf) is the primary component of the alarm pheromone of most aphid species. It is released in response to physical stress including attack by natural enemies and causes aphids to cease feeding and disperse. Eβf also acts as a kairomonal cue for aphid natural enemies. In this study, we collected the headspace volatiles released by aphid colonies of different sizes. Gas chromatography-mass spectrometry analysis demonstrated the presence of Eβf in the absence of predator attack. A quadratic relationship was found between the released ( E )-β-farnesene amounts and aphid colony size. Behavioural impact of aphid alarm pheromone towards Episyrphus balteatus female oviposition behaviour was also demonstrated in this work. These results highlight the primary role of the small but continuous release of aphid alarm pheromone in mechanisms of decision-making by aphid predators during their foraging and egg-laying behaviour.