Do exaptations facilitate mutualistic associations between invasive and native species?

As invasive species are key threats to ecosystem structure and function, it is essential to understand the factors underlying their success. Enigmatically, mutualistic organisms are often successful in colonizing novel environments even though they commonly persist only through intricate relationships with other species. Mutualistic ants, for example, protect aphids from natural enemies while collecting carbohydrate–rich honeydew. To facilitate this interaction, ants have evolved aggressive responses to aphid alarm pheromone emissions. As invasive and native mutualists have not evolved together, however, it is unclear if this form of cross-species communication exists between these two parties thereby facilitating these novel interactions. We address this hypothesis by assessing whether the invasive Argentine ant, Linepithema humile, responds to native poplar aphid, Chaitophorus populicola, alarm signals. Here, we show that interspecific signalling does exist in this newly established mutualistic interaction. Argentine ant workers exhibit increased aggression and double the number of visits to an aphid colony after an aphid alarm signal is emitted. We suggest that pre-adaptations may facilitate the emergence of mutualistic associations between many invasive and native species.     

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.     

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.     

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.     

Learning and signal copying facilitate communication among bird species

Signals relevant to different sets of receivers in different contexts create a conflict for signal design. A classic example is vocal alarm signals, often used both during intraspecific and interspecific interactions. How can signals alert individuals from a variety of other species in some contexts, while also maintaining efficient communication among conspecifics? We studied heterospecific responses to avian alarm signals that drive the formation of anti-predator groups but are also used during intraspecific interactions. In three species-rich communities in the western Himalayas, alarm signals vary drastically across species. We show that, independently of differences in their calls, birds respond strongly to the alarm signals of other species with which they co-occur and much more weakly to those of species with which they do not co-occur. These results suggest that previous exposure and learning maintain heterospecific responses in the face of widespread signal divergence. At an area where only two species regularly interact, one species'' calls incorporate the call of the other. We demonstrate experimentally that signal copying allows strong responses even without previous exposure and suggest that such hybrid calls may be especially favoured when pairwise interactions between species are strong.     

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.     

Chemical Alarm Signals Enhance Survival of Brook Charr (Salvelinus fontinalis) During Encounters with Predatory Chain Pickerel (Esox niger)

A diversity of aquatic organisms release chemical alarm signals when attacked or captured by a predator. These alarm signals are thought to warn other conspecifics of danger and, consequently, may benefit receivers by increasing their survival. Here we experimentally investigated the differences in behaviour and survival of hatchery-reared juvenile brook charr Salvelinus fontinalis that had been exposed to either brook charr skin extract (experimental treatment) or a control of swordtail skin extract (control treatment). Charr exposed to conspecific skin extract exhibited a significant reduction in movement and/or altered their foraging behaviour in the laboratory when compared with charr exposed to swordtail skin extract. We also exposed charr to either water conditioned by a single brook charr disturbed by a predatory bird model or water conditioned by a single undisturbed brook charr. Charr exposed to disturbance signals reduced activity significantly more than charr exposed to chemical stimuli from undisturbed charr. These results demonstrate the existence of both damage-released alarm signals and disturbance signals in brook charr. Wild brook charr also responded to damage-released alarm cues under natural conditions. Charr avoided areas of a stream with minnow traps labelled with conspecific alarm cues vs. control cues. During staged encounters with chain pickerel Esox niger in the laboratory, predator-naive charr fry were better able to evade the predator if they were previously warned by an alarm signal, thus suggesting a survival benefit to receivers. Collectively, these results demonstrate that the presence of alarm signals in brook charr has important implications for understanding predator–prey interactions.     

Aphid alarm pheromone as a cue for ants to locate aphid partners

The mutualistic relationships that occur between myrmecophilous aphids and ants are based on the rich food supply that honeydew represents for ants and on the protection they provide against aphid natural enemies. While aphid predators and parasitoids actively forage for oviposition sites by using aphid semiochemicals, scouts of aphid-tending ant species would also benefit from locating honeydew resources by orienting toward aphid pheromone sources. The present study aims to provide additional information on the use of Aphis fabae alarm pheromone, i.e. (E)-β-farnesene (EβF), by ant scouts. The perception and behavioral impact of EβF on Lasius niger were investigated using electroantennography and two bio-assays measuring their attraction and orientation towards aphid semiochemicals. Pronounced electrical depolarizations were observed from L. niger scout antennae to stimulations of A. fabae alarm pheromone, while other sesquiterpenes elicited weak or no responses. L. niger scouts were significantly attracted toward EβF in a four-arm olfactometer, as well as in an two-choice bioassay. These laboratory results suggest for the first time that low amounts of aphid alarm pheromone can be used by L. niger scouts as a cue indicating the presence of aphid colonies and could therefore mediate the aphid-ant partnership in the field.     

Structure-activity relationships of analogs of the aphid alarm pheromone, (E)-β-farnesene

The structural components essential for activity of the aphid alarm pheromone, (E)-β-farnesene were determined through the synthesis of related farnesene and nor-farnesene analogs. Biological activity was determined with three aphid species belonging to the subfamily Aphidinae. Structural requirements determined to be important for alarm pheromone activity are: The presence of a π-bond (1.34 to 1.39 Å) adjacent to a special free rotational single bond, a (E)-configurational double bond in the central position of the molecule, and a third double bond in the terminal isoprene end of the compound.     

Divergent pheromone-mediated insect behaviour under global atmospheric change

While the effects of global atmospheric changes on vegetation and resulting insect populations(‘bottom‐up interactions’) are being increasingly studied, how these gases modify interactions among insects and their natural enemies (‘top‐down interactions’) is less clear. As natural enemy efficacy is governed largely by behavioural mechanisms, altered prey finding and prey defence may change insect population dynamics. Here we show that pheromone‐mediated escape behaviours, and hence the vulnerability of insects to natural enemies, are divergent under atmospheric conditions associated with global climate change. Chaitophorus stevensis, a common aphid on trembling aspen trees, Populus tremuloides, have diminished escape responses in enriched carbon dioxide (CO₂) environments, while those in enriched ozone (O₃) have augmented escape responses, to alarm pheromone. These results suggest that divergent pheromone‐mediated behaviours could alter predator–prey interactions in future environments.     

Alate production in an aphid in relation to ant tending and alarm pheromone

1. Winged dispersal is vital for aphids as predation pressure and host plant conditions fluctuate. 2. Ant‐tended aphids also need to disperse, but this may represent a cost for the ants, resulting in an evolutionary conflict of interest over aphid dispersal. 3. The combined effects of aphid alarm pheromone, indicating predation risk, and ant attendance on the production of winged aphids were examined in an experiment with Aphis fabae (Homoptera: Aphididae) (Scopoli 1763) aphids and Lasius niger (Formicidae: Formicinae) (Linné, 1758) ants. 4. This study is the first to investigate the joint effects of alarm pheromone and ant attendance, and also the first to detect an influence of alarm pheromone on the production of winged morphs in A. fabae. 5. After a period of 2 weeks, it was found that aphid colonies exposed to intermittent doses of alarm pheromone produced more winged individuals, whereas ant tending had the opposite effect. The effects were additive on a log scale, and ant attendance had a greater proportional influence than exposure to alarm pheromone. A tentative conclusion is that ants have gained the upper hand in an evolutionary conflict about aphid dispersal.     

Spatial organization of the glucosinolate-myrosinase system in brassica specialist aphids is similar to that of the host plant.

Secondary metabolites are important in plant defence against pests and diseases. Similarly, insects can use plant secondary metabolites in defence and, in some cases, synthesize their own products. The paper describes how two specialist brassica feeders, Brevicoryne brassicae (cabbage aphid) and Lipaphis erysimi (turnip aphid) can sequester glucosinolates (thioglucosides) from their host plants, yet avoid the generation of toxic degradation products by compartmentalizing myrosinase (thioglucosidase) into crystalline microbodies. We propose that death, or damage, to the insect by predators or disease causes disruption of compartmentalized myrosinase, which results in the release of isothiocyanate that acts as a synergist for the alarm pheromone E-beta-farnesene.     

Introduced ants reduce interaction diversity in a multi‐species,ant–aphid mutualism

Mutualisms contribute in fundamental ways to the origin, maintenance and organization of biological diversity. Introduced species commonly participate in mutualisms, but how this phenomenon affects patterns of interactions among native mutualists remains incompletely understood. Here we examine how networks of interactions among aphid‐tending ants, ant‐tended aphids, and aphid‐attacking parasitoid wasps differ between 12 spatially paired riparian study sites with and without the introduced Argentine ant Linepithema humile in southern California. To resolve challenges in species identification, we used DNA barcoding to identify aphids and screen for parasitoid wasps (developing inside their aphid hosts) from 170 aphid aggregations sampled on arroyo willow Salix lasiolepis. Compared to uninvaded sites, invaded sites supported significantly fewer species of aphid‐tending ants and ant‐tended aphids. At invaded sites, for example, we found only two species of ant‐tended aphids, which were exclusively tended by L. humile, whereas at uninvaded sites we found 20 unique ant–aphid interactions involving eight species of ant‐tended aphids and nine species of aphid‐tending ants. Ant–aphid linkage density was thus significantly lower at invaded sites compared to uninvaded sites. We detected aphid parasitoids in 14% (28/198) of all aphid aggregations. Although the level of parasitism did not differ between invaded and uninvaded sites, more species of wasps were detected within uninvaded sites compared to invaded sites. These results provide a striking example of how the assimilation of introduced species into multi‐species mutualisms can reduce interaction diversity with potential consequences for species persistence.     

The functional significance of E-β-Farnesene: Does it influence the populations of aphid natural enemies in the fields?

Aphids cause much damage to Chinese cabbage in northern China. Over reliance on pesticides have large environmental and human health costs that compel researchers to seek alternative management tactics for aphid control. The component of aphid alarm pheromone, E-β-Farnesene (EβF), extracted from Matricaria chamomilla L., which attracts natural enemies in the laboratory, may have significant implications for the design of cabbage aphid control strategies. The purpose of this paper is to understand the effects of EβF on natural enemies to cabbage aphid control in Chinese cabbage fields. Ladybeetles on Chinese cabbage leaves in EβF released plots and Aphidiidae in EβF released yellow traps were significantly higher than those of in controls. No significant differences were detected in the interactions of different treatments and the two years for all natural enemies. More important, lower aphid densities were found in EβF released plots. Our results suggested that the EβF extracted from M. chamomilla L. could attract natural enemies to reduce cabbage aphids in the Chinese cabbage fields.     

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.     

Host‐plant genotypic diversity and community genetic interactions mediate aphid spatial distribution

Genetic variation in plants can influence the community structure of associated species, through both direct and indirect interactions. Herbivorous insects are known to feed on a restricted range of plants, and herbivore preference and performance can vary among host plants within a species due to genetically based traits of the plant (e.g., defensive compounds). In a natural system, we expect to find genetic variation within both plant and herbivore communities and we expect this variation to influence species interactions. Using a three‐species plant‐aphid model system, we investigated the effect of genetic diversity on genetic interactions among the community members. Our system involved a host plant (Hordeum vulgare) that was shared by an aphid (Sitobion avenae) and a hemi‐parasitic plant (Rhinanthus minor). We showed that aphids cluster more tightly in a genetically diverse host‐plant community than in a genetic monoculture, with host‐plant genetic diversity explaining up to 24% of the variation in aphid distribution. This is driven by differing preferences of the aphids to the different plant genotypes and their resulting performance on these plants. Within the two host‐plant diversity levels, aphid spatial distribution was influenced by an interaction among the aphid's own genotype, the genotype of a competing aphid, the origin of the parasitic plant population, and the host‐plant genotype. Thus, the overall outcome involves both direct (i.e., host plant to aphid) and indirect (i.e., parasitic plant to aphid) interactions across all these species. These results show that a complex genetic environment influences the distribution of herbivores among host plants. Thus, in genetically diverse systems, interspecific genetic interactions between the host plant and herbivore can influence the population dynamics of the system and could also structure local communities. We suggest that direct and indirect genotypic interactions among species can influence community structure and processes.     

Virus mediated trophic interactions between aphids and their natural enemies

Microbial endosymbionts alter the phenotype of their host which may have cascading effects at both population and community levels. However, we currently lack information on whether the effects of viruses on both host phenotypic traits and host population demography can modify interactions with upper trophic levels. To fill this gap, we investigated whether a prevalent densovirus infecting the aphid Myzus persicae (i.e. MpDNV) can modify trophic interactions between host aphids and their natural enemies (i.e. predators and parasitoids) by influencing aphid phenotypic traits (i.e. body mass and defensive behaviours), population demography (i.e. density and age-structure) and susceptibility towards both predation and parasitism. We found that the virus decreased aphid body mass but did not influence their behavioural defences. At the population level, the virus had a minor effect on aphid adult mortality whereas it strongly reduced the density of nymphs and influenced the stage structure of aphid populations. In addition, the virus enhanced the susceptibility of aphids to parasitism regardless of the parasitoid species. Predation rate on adult aphids was not influenced by the virus but ladybeetle predators strongly decreased the number of aphid nymphs, especially for uninfected ones compared to infected ones. As a result, the virus decreased predator effect on aphid populations. By reducing both aphid quality and availability, increasing their susceptibility to parasitism, and modulating predator effect on aphid populations, we highlighted that viral endosymbionts can be prevalent drivers of their host ecology as they modify their phenotypes and interspecific interactions. These virus-mediated ecological effects may have consequences on enemies foraging strategies as well as trophic webs dynamics and structure.     

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.     

Transgenic disease-resistant wheat does not affect the clonal performance of the aphid Metopolophium dirhodum Walker

Ever since the introduction of transgenic crops one of the main concerns has been their potential impact on non-target organisms. In this study we looked at the impact of transgenic disease-resistant wheat on different clones of the aphid Metopolophium dirhodum. Looking at different clones allowed us to assess whether impacts depended on aphid clone and whether there were aphid clone×wheat line interactions (genotype×environment interactions). The performance of 30 aphid clones on four different transgenic wheat lines and their corresponding control lines was studied in a life-table experiment assessing the following aphid life-history parameters: development time, adult weight, daily fecundity, total offspring number and the fitness estimate F_i′. As expected, we found significant variation among aphid clones for all the measured life-history parameters. However, our experiments did not reveal any major impact of the transgenic wheat lines on aphid performance. The only significant difference was found for total offspring number which was reduced by 3.33% on the transgenic wheat lines compared with the control lines. There was no evidence for a genotype×environment interaction between aphid clones and wheat lines. In sum, our results imply that the genetically modified plants used in this assay were of similar host plant quality as the non-transformed control lines and that the introduced transgene had no major effect on the performance of individual aphid clones.     

Is the (E)‐β‐farnesene only volatile terpenoid in aphids?

Abstract: Herbivore insects use a broad range of chemical cues to locate their host to feed or to oviposit. Whether several plant volatiles are effective allelochemicals for insects, the latter also emit molecules which have infochemical role. The (E)‐β‐farnesene (EBF) is a well‐known aphid alarm pheromone commonly found in all previously tested species. Analysis of the released molecules from 23 aphid species, mainly collected on their natural host plant from May to July, was performed by gas chromatography–mass spectrometry. While EBF was identified as the main volatile substance in 16 species, alone or associated with other molecules, the alarm pheromone was only a minor component of the volatile molecule pattern of five other species. Moreover, two species, Euceraphis punctipennis and Drepanosiphum platanoides, did not release EBF at all but other terpenes were identified. This original observation raised the question on the utility and the source of the non‐EBF volatiles. Are these potential infochemical substances produced by the aphid or only absorbed from the host plant? Here we determined that terpenes released by insects were not only provided by the host plants. Indeed, Megoura viciae emitted additional molecules than the ones from several aphid species reared on the same host plant. Moreover, no systematic relation between the feeding behaviour of the aphid species and the volatile releases was observed. Aphid terpene composition and proportion would provide reliable cues to identify the emitting organism, plant or insect. The next step of this work will be to determine the infochemical role of terpenes found in the range of tested aphid samples to better understand the relations between the different tritrophic levels.