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.     

Entomopathogenic fungi stimulate transgenerational wing induction in pea aphids,Acyrthosiphon pisum (Hemiptera: Aphididae)

1. Aphid natural enemies include not only predators and parasitoids but also pathogens, of which fungi are the most studied for biological control. While wing formation in aphids is induced by abiotic conditions, it is also affected by biotic interactions with their arthropod natural enemies. Wing induction via interactions with arthropod natural enemies is mediated by the increase in their physical contact when alarmed (pseudo‐crowding). Pathogenic fungi do not trigger this alarm behaviour in aphids and, therefore, no pseudo‐crowding occurs. 2. We hypothesise that, while pathogenic fungi will stimulate maternally induced wing formation, the mechanism is different and is influenced by pathogen specificity. We tested this hypothesis using two entomopathogenic fungi, Pandora neoaphidis and Beauveria bassiana, an aphid specialist and a generalist respectively, on the pea aphid, Acyrthosiphon pisum Harris. 3. We first demonstrate that pea aphids infected with either pathogen and maintained in groups on broad bean plants produced a higher proportion of winged morphs than uninfected control aphids. We then show that, when maintained in isolation, aphids infected with either pathogen also produced higher proportions of winged offspring than control aphids. There was no difference between P. neoaphidis and B. bassiana in their effects on wing induction in either experiment. 4. Unlike the effect of predators and parasitoids on pea aphid wing induction, the effect of pathogens is independent of physical contact with other aphids, suggesting that physiological cues induce wing formation in infected aphids. It is possible that aphids benefit from wing induction by escaping infected patches whilst pathogens may benefit through dispersion. Possible mechanisms of wing induction are discussed.     

Transgenerational phenotypic plasticity under future atmospheric conditions

Organisms often exhibit transgenerational phenotypic changes in response to an increased risk of parasitism or predation. Shifts in global atmospheric composition could modify these phenotypic effects through changes in either nutrient quantity/quality or altered interactions with higher trophic levels. Here we show that future atmospheric conditions alter a natural enemy‐induced wing polyphenism in aphids. Winged offspring production by Uroleucon nigrotuberculatum aphids on goldenrod (Solidago canadensis var. scabra) does not differ in enriched CO₂ and/or O₃ atmospheres. However, proportionally more winged offspring are produced in response to search cues from both coccinellid predators (Coccinella septempunctata) and hymenopteran parasitoids (Aphidius polygonaphis) relative to plants not searched by natural enemies. Moreover, the magnitude of this response differs under enriched CO₂ and O₃ environments. Aphids produce more winged offspring in response to predators under elevated CO₂, but produce more winged offspring in response to parasitoids under elevated O₃. Thus, global atmospheric changes influence natural enemy‐mediated phenotypic expression, with potentially far‐reaching consequences for trophic dynamics.     

Predator-induced morphological shift in the pea aphid

Aphids exhibit a polymorphism whereby individual aphids are either winged or unwinged. The winged dispersal morph is mainly responsible for the colonization of new plants and, in many species, is produced in response to adverse environmental conditions. Aphids are attacked by a wide range of specialized predators and predation has been shown to strongly influence the growth and persistence of aphid colonies. In two experiments, we reared two clones of pea aphid (Acyrthosiphon pisum) in the presence and absence of predatory ladybirds (Coccinella septempunctata or Adalia bipunctata). In both experiments, the presence of a predator enhanced the proportion of winged morphs among the offspring produced by the aphids. The aphid clones differed in their reaction to the presence of a ladybird, suggesting the presence of genetic variation for this trait. A treatment that simulated disturbance caused by predators did not enhance winged offspring production. The experiments indicate that aphids respond to the presence of a predator by producing the dispersal morph which can escape by flight to colonize other plants. In contrast to previous examples of predator-induced defence this shift in prey morphology does not lead to better protection against predator attack, but enables aphids to leave plants when mortality risks are high.     

Aphid Wing Induction and Ecological Costs of Alarm Pheromone Emission under Field Conditions

The pea aphid, Acyrthosiphon pisum Harris, (Homoptera: Aphididae) releases the volatile sesquiterpene (E)-β-farnesene (EBF) when attacked by a predator, triggering escape responses in the aphid colony. Recently, it was shown that this alarm pheromone also mediates the production of the winged dispersal morph under laboratory conditions. The present work tested the wing-inducing effect of EBF under field conditions. Aphid colonies were exposed to two treatments (control and EBF) and tested in two different environmental conditions (field and laboratory). As in previous experiments aphids produced higher proportion of winged morphs among their offspring when exposed to EBF in the laboratory but even under field conditions the proportion of winged offspring was higher after EBF application (6.84±0.98%) compared to the hexane control (1.54±0.25%). In the field, the proportion of adult aphids found on the plant at the end of the experiment was lower in the EBF treatment (58.1±5.5%) than in the control (66.9±4.6%), in contrast to the climate chamber test where the numbers of adult aphids found on the plant at the end of the experiment were, in both treatments, similar to the numbers put on the plant initially. Our results show that the role of EBF in aphid wing induction is also apparent under field conditions and they may indicate a potential cost of EBF emission. They also emphasize the importance of investigating the ecological role of induced defences under field conditions.     

The influence of natural enemies on wing induction in Aphis fabae and Megoura viciae (Hemiptera: Aphididae)

Previous studies have shown that the aphid species, Aphis fabae Scopoli and Megoura viciae Buckton, do not produce winged offspring in the presence of natural enemies, in contrast to results for the pea aphid (Acyrthosiphon pisum (Harris)) and the cotton aphid (Aphis gossypii Glover); but these studies did not involve exposing aphids directly to natural enemies. We exposed colonies of both A. fabae and M. viciae to foraging lacewing (Chrysoperla carnea (Stephens)) larvae and found that the predators did not induce winged morphs among offspring compared to unexposed controls. Colonies of A. fabae responded to an increase in aphid density with increasing winged morph production, while such response was not found for M. viciae. We suggest that different aphid species differ in their susceptibility to natural enemy attack, as well as in their sensitivity to contact.     

Non-additive effects of multiple natural enemies on aphid populations

The question of whether multiple natural enemies often interact to produce lower host mortality than single enemies acting alone has not yet been resolved. We compared the effects of four different combinations of natural enemies-parasitoids, predators, parasitoids plus predators, and no enemies-on caged aphid populations on marsh elder, Iva frutescens, in west-central Florida. Using starting densities of natural enemies commonly found in the field, we showed that parasitoid wasps reduced aphid population densities more than predatory ladybird beetles. The addition of predators to cages containing parasites reduced the ability of parasitoids to decrease aphid population densities. Because the experiments ran only over the course of one generation, such a reduction in the effectiveness of parasites is likely caused by interference of predators with parasitoid behavior. Parasitism in the cages containing both parasitoids and predators was reduced when compared to percent parasitism in parasitoid-only cages, but this could also be due to predation. Our experiments showed that ladybird beetles prey on parasitized aphids. Thus over the long-term, the effectiveness of parasites is impaired by the interference of predators on ovipositing parasitoids and by the predation of parasitized aphids. The effects of natural enemies in this system are clearly non-additive.     

The role of natural enemy guilds in Aphis glycines suppression

Generalist natural enemy guilds are increasingly recognized as important sources of mortality for invasive agricultural pests. However, the net contribution of different species to pest suppression is conditioned by their biology and interspecific interactions. The soybean aphid, Aphis glycines (Hemiptera: Aphididae), is widely attacked by generalist predators, but the relative impacts of different natural enemy guilds remains poorly understood. Moreover, low levels of A. glycines parasitism suggest that resident parasitoids may be limited through intraguild predation. During 2004 and 2005, we conducted field experiments to test the impact of different guilds of natural enemies on A. glycines. We contrasted aphid abundance on field cages with ambient levels of small predators (primarily Orius insidiosus) and parasitoids (primarily Braconidae), sham cages and open controls exposed to large predators (primarily coccinellids), and cages excluding all natural enemies. We observed strong aphid suppression (86- to 36-fold reduction) in treatments exposed to coccinellids, but only minor reduction due to small predators and parasitoids, with aphids reaching rapidly economic injury levels when coccinellids were excluded. Three species of resident parasitoids were found attacking A. glycines at very low levels (<1% parasitism), with no evidence that intraguild predation by coccinellids attenuated parasitoid impacts. At the plant level, coccinellid impacts resulted in a trophic cascade that restored soybean biomass and yield, whereas small natural enemies provided only minor protection against yield loss. Our results indicate that within the assemblage of A. glycines natural enemies in Michigan, coccinellids are critical to maintain aphids below economic injury levels.     

<Emphasis Type="Italic">Aphidius ervi</Emphasis> Preferentially Attacks the Green Morph of the Pea Aphid, <Emphasis Type="Italic">Acyrthosiphon pisum</Emphasis>

The pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae) is found in red and green color morphs. Previous work has suggested that the aphidiine parasitoid Aphidius ervi Haliday preferentially attacks green pea aphids in the field. It is not clear whether these results reflect a real preference, or some unknown clonal difference, such as in immunity, between the aphids used in the previous studies. We used three susceptibility-matched pairs of red and green morph pea aphid clones to test for preferences. In a no-choice situation, the parasitoids attacked equal proportions of each color morph. When provided with a choice, A. ervi was significantly more likely to oviposit into colonies formed from green morphs when the neighboring colony was formed from red morph aphids. In contrast, red morphs were less likely to be attacked when their neighboring colony was of the green morph. By preferentially attacking green colonies, A. ervi may reduce the likelihood of intraguild predation, as it is suggested that visually foraging predators preferentially attack red aphid colonies. Furthermore, if this host choice behavior is replicated in the field, we speculate that color morphs of the pea aphid may interact indirectly through their shared natural enemies, leading to intraspecific apparent competition.     

The interplay between density- and trait-mediated effects in predator-prey interactions: a case study in aphid wing polymorphism

Natural enemies not only influence prey density but they can also cause the modification of traits in their victims. While such non-lethal effects can be very important for the dynamic and structure of prey populations, little is known about their interaction with the density-mediated effects of natural enemies. We investigated the relationship between predation rate, prey density and trait modification in two aphid-aphid predator interactions. Pea aphids (Acyrthosiphon pisum, Harris) have been shown to produce winged dispersal morphs in response to the presence of ladybirds or parasitoid natural enemies. This trait modification influences the ability of aphids to disperse and to colonise new habitats, and hence has a bearing on the population dynamics of the prey. In two experiments we examined wing induction in pea aphids as a function of the rate of predation when hoverfly larvae (Episyrphus balteatus) and lacewing larvae (Chrysoperla carnea) were allowed to forage in pea aphid colonies. Both hoverfly and lacewing larvae caused a significant increase in the percentage of winged morphs among offspring compared to control treatments, emphasising that wing induction in the presence of natural enemies is a general response in pea aphids. The percentage of winged offspring was, however, dependent on the rate of predation, with a small effect of predation on aphid wing induction at very high and very low predation rates, and a strong response of aphids at medium predation rates. Aphid wing induction was influenced by the interplay between predation rate and the resultant prey density. Our results suggests that density-mediated and trait-mediated effects of natural enemies are closely connected to each other and jointly determine the effect of natural enemies on prey population dynamics.     

Body colour and genetic variation in winged morph production in the pea aphid

Aphids (Homoptera: Aphidoidea) produce a number of different phenotypes in their life-cycle, among which are winged (alate) and wingless (apterous) morphs. Lowe & Taylor (1964) and Sutherland (1969a, b) were the first to suggest that aphid clones differ in their propensity to produce the winged morph and that in the pea aphid (Acyrthosiphon pisum Harris), this propensity is linked to the colour of the phenotype. We tested for the occurrence of genetic variation in winged morph production by rearing individuals from red and green clones of pea aphid under wing-inducing (crowding) and control conditions, and scored the phenotypes of their offspring. Clones differed significantly in alate production and red clones produced on average a higher proportion of winged morphs than green clones. Importantly, however, there was considerable variation between clones of the same colour. Broad-sense heritabilities of winged morph production were 0.69 (crowding treatment) and 0.63 (control). Clones also differed in the number of offspring they produced. When exposed to the crowding stimulus, aphids deferred offspring production, resulting in a higher number of offspring produced in the crowding treatment than in the control.     

Colony growth and dispersal in the ant-tended aphid, <Emphasis Type="Italic">Aphis craccivora</Emphasis> Koch,and the non-ant-tended aphid, <Emphasis Type="Italic">Acyrthosiphon pisum</Emphasis> Harris,under the absence of predators and ants

To elucidate the potential for colony growth and the dispersal of aphids in relation to the ant attendance, the mobility, tolerance of starvation, colony growth, and dispersal were examined in the ant-tended Aphis craccivora Koch and the non-ant-tended Acyrthosiphon pisum Harris under the absence of predators and ants. The increase of the dispersal rate with density was more conspicuous in Ac. pisum than Ap. craccivora. The success rate of dispersal was higher in Ac. pisum than Ap. craccivora. These results would be derived from the higher ability of dispersal by walking in Ac. pisum than Ap. craccivora. The longer legs, higher walking speed, and stronger tolerance of starvation in Ac. pisum might result in a higher ability of dispersal by walking. These traits may have developed in relation to non-ant attendance, because Ac. pisum aphids frequently escape from natural enemies by dropping from the host plant. On the other hand, Ap. craccivora have not developed morphological and behavioral traits concerning dispersal by walking, because increasing colony size without dispersal is likely to be advantageous for ant attraction. Escaping behaviors of Ap. craccivora from natural enemies have not been well developed due to the ant’s defense against natural enemies. The proportion of alatae in Ap. craccivora was higher than in Ac. pisum instead of a lesser ability for dispersal by walking in Ap. craccivora. The differences in ant attendance have been influenced in the development of morphological and behavioral traits concerning the dispersal ability, and then, different potentials for reproduction and dispersal have developed in ant-tended aphids and non-ant-tended aphids.     

Juvenile hormone titres and winged offspring production do not correlate in the pea aphid, Acyrthosiphon pisum

Pea aphids, Acyrthosiphon pisum, reproduce parthenogenetically and are wing-dimorphic such that offspring can develop into winged (alate) or unwinged (apterous) adults. Alate induction is maternal and offspring phenotype is entirely determined by changes in the physiology and environment of the mother. Juvenile hormones (JHs) have been implicated in playing a role in wing differentiation in aphids, however until recently, methods were not available to accurately quantify these insect hormones in small insects such as aphids. Using a novel LC-MS approach we were able to quantify JH III in pea aphids that were either producing a high proportion of winged morphs among their offspring or mainly unwinged offspring. We measured JH III titres by pooling the hemolymph of 12 or fewer individuals (1 μL hemolymph) treated identically. Levels of JH ranged from 30 to 163 pg/μL. While aphids in the two treatments strongly differed in the proportion of winged morphs among their offspring, their JH III titres did not differ significantly. There was also no correlation between JH III titre and the proportion of winged offspring in induced aphids. This supports earlier findings that wing dimorphism in aphids may be regulated by other physiological mechanisms.     

Comparison of the wing polyphenic response of pea aphids (Acyrthosiphon pisum) to crowding and predator cues

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Endophytic fungi decrease available resources for the aphid Rhopalosiphum padi and impair their ability to induce defences against predators

Abstract.  1. The production of winged morphs is a well known mechanism of induced defence in aphids to escape from natural enemies, and is also a reaction to poor resource quality.
2. Host plants of aphids often associate with endophytic fungi that have been shown to reduce the fitness of some species of aphids.
3. It was hypothesised that endophyte infection of host plants that represent a low quality plant resource should increase the aphid's induced response to a predator because both low plant quality and predator presence represent a stronger cue for wing production than predator presence alone.
4. In a laboratory experiment, bird cherry-oat aphids Rhopalosiphum padi L. were exposed to the factors predator threat and endophyte infection and the effects of these factors on the proportion of winged morphs produced by the aphid colonies was analysed.
5. The presence of endophytic fungi strongly decreased aphid colony sizes. When a predator threat was present, all colonies on endophyte-free grasses produced winged morphs whereas only a few colonies were able to produce winged morphs on endophyte-infected grasses. However, these few colonies produced larger proportions of winged morphs than colonies on endophyte-free grasses. Without a predator threat, no colonies on endophyte-infected grasses produced any winged morphs.
6. These results show that aphids in stressed conditions and with reduced fitness will only invest in inducible defences when predators are present but are unable to produce winged morphs in response to endophyte presence.     

Ecological considerations for biological control of aphids in protected culture

Several braconid and aphelinid parasitoids, midges, lacewings, and ladybird beetles are used to control aphids in greenhouses. Here, I review three topics as ecological bases for the biological control of aphids in a protected culture: the preliminary evaluation of biological control agents, natural enemy release strategies, and the effects of intraguild predation (IGP) on biological control. A comparison of several parasitoid species was conducted to select agents for the biological control of aphids; the intrinsic rate of natural increase was a useful criterion in the preliminary evaluation. To compare predators as biological control agents, the aphid-killing rate must be considered as a critical criterion, rather than reproductive criteria. The banker plant system (open rearing system) is used as a release method for Aphidius colemani and other natural enemies of aphids. Continuous release of parasitoid adults, which is the important characteristic of this method, has a stabilizing effect on population fluctuation in the aphid–parasitoid system. Two species of natural enemies can be used to control aphids in greenhouses. When one parasitoid and one predator are used simultaneously in a greenhouse, IGP of the parasitoid by the predator can occur, but the effect of IGP is less important in greenhouses than in the field.     

Altered dispersal behaviour in parasitised aphids: parasitoid-mediated or pathology?

1. Several hypotheses concerning modified dispersal behaviour in aphids parasitised by aphidiine wasps (Hymenoptera: Braconidae: Aphidiinae) were tested in the laboratory. Behavioural changes may be host-mediated, parasitoid-mediated, or a by-product of trauma and pathology. 2. Mummification site varied with parasitoid species. Pea aphids (Acyrthosiphon pisum) parasitised by Aphidius ervi, Aphidius pisivorus, Monoctonus paulensis, and Praon pequodorum mummified near the aphids’ preferred feeding sites on bean plants, but those parasitised by Ephedrus californicus often died and mummified outside the colony, away from the plants. 3. Parasitism by E. californicus had a progressive effect on the behaviour of pea aphids. Approaching death, aphids lost motor control and frequently dropped off the host plant when disturbed. Dropped aphids were unable to return to the feeding site and mummified elsewhere. The proportion of aphids mummifying outside the colony increased with mummy density. 4. Mummification site was not influenced by the presence within the same colony of aphids parasitised by different species of aphidiine wasps. 5. The evidence does not support the hypothesis that mummification site selection in E. californicus is determined by a host- or a parasitoid-mediated change in aphid dispersal behaviour. Association-specific differences in the dynamics of larval development and growth between aphidiine species provide an equally valid and possibly more general explanation of mummification behaviour.     

Cascading effects of herbivore protective symbionts on hyperparasitoids

1. Microbial symbionts can play an important role in defending their insect hosts against natural enemies. However, researchers have little idea how the presence of such protective symbionts impacts food web interactions and species diversity. 2. This study investigated the effects of a protective symbiont (Hamiltonella defensa) in pea aphids (Acyrthosiphon pisum) on hyperparasitoids, which are a trophic level above the natural enemy target of the symbiont (primary parasitoids). 3. Pea aphids, with and without their natural infections of H. defensa, were exposed first to a primary parasitoid against which the symbiont provides partial protection (either Aphidius ervi or Aphelinus abdominalis), and second to a hyperparasitoid known to attack the primary parasitoid species. 4. It was found that hyperparasitoid hatch rate was substantially affected by the presence of the symbiont. This effect appears to be entirely due to the removal of potential hosts by the action of the symbiont: there was no additional benefit or cost experienced by the hyperparasitoids in response to symbiont presence. The results were similar across the two different aphid–parasitoid–hyperparasitoid interactions we studied. 5. It is concluded that protective symbionts can have an important cascading effect on multiple trophic levels by altering the success of natural enemies, but that there is no evidence for more complex interactions. These findings demonstrate that the potential influence of protective symbionts on the wider community should be considered in future food web studies.     

Regulation of wing formation and adult development in an aphid host, Aphis fabae, by the parasitoid Aphidius colemani

Nymphs of presumptive winged gynoparae of Aphis fabae (Hemiptera: Aphididae), were exposed to female parasitoids, Aphidius colemani (Hymenoptera: Aphidiidae) and stung once with the ovipositor. Wing development was inhibited and, when aphids were parasitised during the early stages, they did not reach the adult stage but mummies with rudimentary or no wingbuds are observed in the host's fourth-stadium. These and previous studies have suggested that wing development may be inhibited by factor(s) from the maternal parasitoid injected into the host at the time of oviposition. In an attempt to identify such factor(s), saline extracts of whole female parasitoids, abdomens, ovaries and venom glands were prepared. When a saline extract of venom glands was injected into late-second-stadium aphids, many develop to fourth-stadium nymphs with rudimentary wingbuds, indicating an effect on wing formation but also showed developmental arrest and often died when attempting to moult to the adult stage. It appears that host death may be related to physiological/biochemical interactions of parasitoid and host rather than just late stage parasitoid larvae ingesting the host's vital organs. Injections with extracts into later host stadia gave similar results with regard to development to the adult, although aphids injected in the late-fourth-stadium develop normally to the adult stage with no effect on wing formation. The results indicate that the earlier the injection before the final moult the greater the effect of the injected extract on preventing adult development.Extracts prepared from head + thorax do not affect aphid development and the results indicate that there is an active factor(s) - likely a protein - in the female parasitoid's venom that disrupts wing development and/or inhibits development to the adult stage. Surprisingly, injections of extracts from male parasitoids have similar effects but the location and function of such a factor(s) in males are unknown.     

Floral diversity, parasitoids and hyperparasitoids – A laboratory approach

Adding floral resources to agro-ecosystems to improve biological control can enhance the survival, egg load, and parasitism rate of insect parasitoids. However, this may not always be the case because the herbivore may benefit from the added resource as much as, or more than the third-trophic level. In addition, the natural enemies of those in the third-trophic level may also derive improved fitness from the added resources. Both these processes will dampen trophic cascades, leading to less-effective biological control. In this study, the effect of adding different flowering plants on the longevity, egg load, aphid parasitism rates and hyperparasitism of Aphidius ervi Haliday (Hymenoptera: Braconidae) by its hyperparasitoid Dendrocerus aphidum Rondani (Hymenoptera: Megaspilidae) were investigated, using the pea aphid Acyrthosiphon pisum Harris (Homoptera: Aphididae) as the herbivore. Parasitoids exposed to buckwheat survived, on average, between four to five times as long as those in the control (water) and those in phacelia, alyssum and coriander treatments survived three to four times as long. Hyperparasitoids exposed to buckwheat survived five to six times as long as those in the control and three to five times longer with the other plants compared with the control. Almost all flower species significantly increased parasitoid and hyperparasitoid egg loads and the number of parasitised aphids and parasitised mummies compared with control. Understanding the factors influencing the dynamics of multitrophic interactions involving flowering plants, herbivores, parasitoids and hyperparasitoids is a fertile area for future research. One of the most challenging areas in contemporary ecology concerns the relative importance of different types of biodiversity mediating trophic interactions and thereby influencing the structure of communities and food webs. This paper begins to explore this using an experimental, laboratory-based approach.