Foraging by the carabid Agonum dorsale in the field

Abstract. 1. Small arenas in the field were used for observing adult Agonum dorsale (Pont.) foraging in a wheat crop.
2. The carabid showed no significant change in behaviour between low and high aphid density arenas.
3. Individuals foraged nocturnally and spent most of their time on the ground searching for prey. They climbed infrequently and then not high enough to reach aphid aggregations on the ears and flag leaves of wheat.
4. Gut dissection showed that more individuals had eaten aphids in the high aphid density arena than the low. Recording of aphid distribution within the arenas showed that this increase in aphid consumption could be explained by A.dorsale capturing aphids on the ground. Prey availability per unit area was in fact higher on the ground than on the wheat.
5. The contribution of ground-zone predators such as A.dorsale to the control of cereal aphids will be determined by the frequency with which aphids arrive on the ground and the proportion of these which reclimb the wheat and reproduce in the absence of predation.     

Foliar and ground-foraging predators of aphids associated with alfalfa crops in Chile: Are they good or bad partners?

Carabids and coccinellids are the most abundant aphid predators in alfalfa. Depending on the amount of prey consumed, the impact of their combined effect can be additive, antagonistic, or synergistic. Laboratory trials demonstrated that a higher proportion of Aphis craccivora Koch dropped from the alfalfa plants in the presence of coccinellids, and that the interaction between these predators was additive or synergistic, but never antagonistic, suggesting that they might be good partners in controlling aphids.     

The economics of escape behaviour in the pea aphid,Acyrthosiphon pisum

Summary Pea aphids have several alternative responses to the detection of alarm pheromone produced by conspecifics. One of these, dropping from the feeding site to the ground, is potentially costly owing to the risk of desiccation-induced mortality on the ground before another host plant can be reached. Both dropping and walking from the feeding site incur a cost due to lost feeding opportunity. The aphids' decision as to which anti-predator tactic to use should be sensitive to the costs of their behaviour. Consequently, aphids should be less likely to drop when the risk of desiccation is higher, and less likely to drop or walk when the lost opportunity cost is higher. We tested these predictions by manipulating climatic severity (temperature and humidity) and host quality, respectively. As predicted, aphids are less likely to drop or walk in response to pheromone when feeding on high quality than on low quality hosts, and less likely to drop when the environment is hot and dry than when it is more benign. The latter is true whether the aphids are feeding on real or simulated leaves. Since all aphids were of the same clone, these results show that individual aphid genotypes possess the ability to adaptively modify their escape behaviour with changes in prevailing conditions. A number of other behavioural observations in the aphid literature may be interpreted in an economic or cost-benefit framework. The approach holds considerable promise for understanding many aspects of the anti-predator behaviour of aphids and other animals.     

Effects of aphids on foliar foraging by Argentine ants and the resulting effects on other arthropods

Abstract.  1. Although interactions between ants and honeydew-producing insects have received considerable study, relatively little is known about how these interactions alter the behaviour of ants in ways that affect other arthropods. In this study, field and greenhouse experiments were performed that examined how the presence of aphids ( Aphis fabae solanella ) on Solanum nigrum influenced the foraging behaviour of Argentine ants ( Linepithema humile ) and, in turn, modified the extent to which ants deter larval lacewings ( Chrysoperla rufilabris ), which are known aphid predators.
2. A field experiment demonstrated that the level of foliar foraging by ants increased linearly with aphid abundance, whereas no relationship existed between the level of ground foraging by ants and aphid abundance.
3. In the greenhouse, as in the field, foliar foraging by ants greatly increased when aphids were present. Higher levels of foliar foraging led to a twofold increase in the likelihood that ants contacted aphid predators. As a result of these increased encounters with ants, lacewing larvae were twice as likely to be removed from plants with aphids compared with plants without aphids. Once contact was made, however, the behaviour of ants towards lacewing larvae appeared similar between the two experimental groups.
4. Argentine ants drive away or prey upon a diversity of arthropod predators and parasitoids, but they also exhibit aggression towards certain herbivores. Future work should attempt to quantify how the ecological effects that result from interactions between honeydew-producing insects and invasive ants, such as L. humile , differ from those that result from interactions between honeydew-producing insects and native ants.     

Host Location by Apterous Aphids After Escape Dropping from the Plant

In response to approaching enemies aphids may drop from their host plant to the ground. The risk of predation on the ground, desiccation and host loss, create the need for efficient host location by the dropping aphids. Most studies have focused on the factors that influence dropping behavior; only a few have addressed host location after dropping from the plant. We assessed post-dropping behavior in apterous Macrosiphoniella artemisiae (Boyer de Fonscolombe) (Aphididae), which feed on Artemisia arborescens L. Vibration of the apical bud induced dropping in 36% of the colony members. Dropping rates were highest in mature aphids (63%). In the experimental arena (without ground predators), nearly all mature aphids that were dropped 13 cm from the plant, found their way back in ca. 40 s. The location process may be based on visual cues, as M. artemisiae is capable of visually discriminating between host and non-host targets and apparently does not react to volatiles emitted from the plant.     

The effect size of aphid‐tending ants in an agricultural tri‐trophic system

Most studies regarding ant–aphid interactions focus only on the direct effects of ants on tended aphids and aphidophagous predators, or the indirect effects on the host plant. Studies evaluating the effects of aphid‐tending ants on more than one trophic level are rare and evaluate only the presence or absence of such effects. Here we assessed the effect sizes of ants in a tri‐trophic system (common bean plants, aphids and lacewing larvae). We tested if the presence of aphid‐tending ants has positive effects on aphid abundance and host‐plant production and negative effects on aphid predator abundance. We also hypothesized that aphid‐tending ants affect more intensely trophic levels that are more directly related to them (i.e., first aphids, then aphid predators and then host plants). We tested these hypotheses in field mesocosms experiments using the presence and absence of ants. We found that aphid‐tending ants have great positive effects on final aphid abundance. Ants also positively affected the number of seeds; however, it was not possible to measure the effect size for this trophic level. Furthermore, ants had negative effects on lacewing larvae only at first release. The effect size of ants was greater for aphids, followed by lacewing larvae, and with no effects on the number of seeds produced. Ants positively affect aphids and host‐plant production, probably by way of honeydew collection preventing the development of entomophagous/saprophytic fungi. On the other hand, ants negatively affect lacewing larvae by excluding them from the host plant. In natural systems, several ant species may attend aphids, differently affecting the organisms of the various trophic levels within the ant–aphid interaction, thereby obscuring the real effect size of ants. Assessing the effect size of aphid‐tending ants on the organisms involved in ant–aphid interactions provides more realistic information about the effects of this interaction on natural systems.     

Facultative symbionts are associated with host plant specialization in pea aphid populations

The pea aphid, Acyrthosiphon pisum, shows significant reproductive isolation and host plant specialization between populations on alfalfa and clover in New York. We examine whether specialization is seen in pea aphids in California, and whether fitness on alternative host plants is associated with the presence of bacterial symbionts. We measured the fitness of alfalfa- and clover-derived aphids on both types of plants and found no evidence for specialization when all aphid lineages were considered simultaneously. We then screened all aphids for the presence of four facultative bacterial symbionts: PAR, PASS, PABS and PAUS. Aphids with PAUS were host-plant specialized, having twice as many offspring as other aphids on clover, and dying on alfalfa. Other aphids showed no evidence of specialization. Additionally, aphids with PABS had 50% more offspring than aphids with PASS when on alfalfa. Thus, specialist and generalist aphid lineages coexist, and specialization is symbiont associated. Further work will resolve whether PAUS is directly responsible for this variation in fitness or whether PAUS is incidentally associated with host-plant specialized aphid lineages.     

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.     

Predation of the cereal aphid Sitobion avenae by polyphagous predators on the ground

Abstract. 1. Polyphagous predator densities were manipulated in a wheat crop using polythene exclusion barriers.
2. The rates at which aphids fell to the ground and subsequently climbed and returned to the crop canopy were measured.
3. Peak aphid density was highest when polyphagous predator density was lowest.
4. Similar rates of aphid fall-off were measured in each plot, but aphid climbing rate was highest when predator densities were lowest.
5. It was concluded that ground-zone predators reduced the rate at which aphids return to the crop canopy.     

Predation Determines Different Selective Pressure on Pea Aphid Host Races in a Complex Agricultural Mosaic

Field assessments were conducted to examine the interplay between host plant and predation in complex agricultural mosaic on pea aphid clover and alfalfa races. In one experiment, we examined the relative fitness on clover race (CR) and alfalfa race (AR) pea aphids on broad bean, red clover and alfalfa alone. But because clover is typically grown in a more complex agricultural mosaic with alfalfa and broad bean, a second experiment was conducted to assess the fitness consequences under predation in a more complex agricultural field setting that also included potential apparent competition with AR pea aphids. In a third experiment we tested for the effect of differential host race density on the fitness of the other host race mediated by a predator effect. CR pea aphids always had fitness losses when on broad bean (had lower fitness on broad bean relative to red clover) and fitness benefits when on red clover (higher fitness on red clover relative to broad bean), whether or not in apparent competition with alfalfa race aphids on bean and alfalfa. AR suffered fitness loss on both alfalfa and bean in apparent competition with CR on clover. Therefore we can conclude that the predation rate between host races was highly asymmetrical. The complexity of the agricultural mosaic thus can influence prey selection by predators on different host plants. These may have evolutionary consequences through context dependent fitness benefits on particular host plants.     

Pea aphid dropping behavior diminishes foraging efficiency of a predatory ladybeetle

Antipredator defensive behaviors are a well‐studied and often crucial part of prey life histories, but little has been done to quantify how such behaviors affect natural enemies, their foraging, and their effectiveness as biological control agents. We explored how the generalist predatory coccinellid Harmonia axyridis Pallas (Coleoptera: Coccinellidae) affects the dropping behavior of the pea aphid, Acyrthosiphon pisum (Harris) (Homoptera: Aphididae), and in turn, how that defensive behavior affects the foraging efficiency of the predator. Experimental arenas that allowed or prevented pea aphid dropping were compared to determine how dropping influences the foraging of multiple life stages of H. axyridis: second instars, fourth instars, and adults. Dropping reduced predation on aphids by all ladybeetle life stages. Despite older predators inducing more dropping, aphid dropping reduced predation by approximately 40% across all ladybeetle life stages. Aphid dropping and predator consumption of aphids were both correlated with how much the predator moved, which also increased with predator life stage. We suggest that the high rates of dropping induced by H. axyridis and the subsequent decrease in H. axyridis foraging efficiency may partially explain why H. axyridis is less effective at controlling pea aphids than it is at controlling other aphid species that do not drop.     

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.     

Contact with the host plant enhances aphid survival at low temperatures

1. The hypothesis, suggested by previous studies, that host plant contact reduces the cold tolerance of anholocyclic aphids was tested under laboratory conditions. Adult and first-instar Rhopalosiphum padi (L.) were exposed to temperatures of 0, –5 and –10 °C on intact plants, excised leaves and in the absence of contact with plant material.
2. Median lethal time (LT₅₀) values at all three temperatures indicate that aphids exposed in association with plant material survive longer than aphids that have no contact with their host plant. The difference in survival was most pronounced at –10 °C. Therefore, the above hypothesis is rejected for aphids on cereals because host plant contact apparently enhances cold tolerance.
3. Exposure on excised leaves also enhanced aphid survival at low temperature but was less effective than the intact plant. This suggests that plant quality as well as the presence or absence of plants is important in the cold tolerance of aphids on cereals.     

Dropping behaviour of larvae of aphidophagous ladybirds and its effects on incidence of intraguild predation: interactions between the intraguild prey, Adalia bipunctata (L.) and Coccinella septempunctata (L.), and the intraguild predator, Harmonia axyridis Pallas

Abstract.  1. Two experiments were performed in the laboratory to assess the behaviour of dropping from a host plant as a defence against intraguild predation in aphidophagous ladybird larvae.
2. In the first experiment, encounters were observed on bean plants between fourth instars of the intraguild predator species, Harmonia axyridis , and first instars of two other ladybird species, Adalia bipunctata (L.) and Coccinella septempunctata (L.). The percentages of first instars of the latter two species that dropped from the plant in response to attack differed dramatically, with 47.5% of C. septempunctata first instars dropping vs. 0% of A. bipunctata .
3. In the second experiment, first instars of A. bipunctata or C. septempunctata and a fourth instar of H. axyridis were allowed to forage together on bean plants for 3 h. During this time, 44.3% of C. septempunctata larvae dropped from the plant, but less than 2% of A. bipunctata larvae did so. In contrast, 95.0% of A. bipunctata larvae fell victim to intraguild predation by H. axyridis vs. only 54.5% of C. septempunctata larvae.
4. The significance of dropping behaviour of ladybird larvae as a defence against intraguild predation, and the relationship of dropping behaviour to species-specific habitat affinity of ladybirds, is discussed.     

The use of visual cues in host evaluation by aphidiid wasps

We examined host evaluation behaviour in three species of aphid parasitoids, Ephedrus californicus Baker, Monoctonus paulensis (Ashmead), and Praon pequodorum Viereck (Hymenoptera: Aphidiidae). Mated females were provided with pairwise choices among three kinds of hosts in the laboratory: (green) pea aphid, Acyrthosiphon pisum (Harris), and a green and a pink colour morph of alfalfa aphid, Macrosiphum creelii Davis. Patterns of attack and host acceptance were species-specific. Females of E. californicus did not respond to the presence of aphids prior to making antennal contact. Variations in rates of parasitization (pea aphid>green alfalfa aphid>pink alfalfa aphid) were consistent with differences in aphid defensive behaviours; no ‘preference’ for any host type was evident when aphids were anaesthetized with carbon dioxide. In M. paulensis, the order of preference (pea aphid>green alfalfa aphid>pink alfalfa aphid) did not vary when aphids were immobilized, or presented in the dark, or both. Host movement did not influence the rate of attack by M. paulensis. In contrast, the ranked order of preference in P. pequodorum varied with circumstance. In the light, females attacked pea aphid and green alfalfa aphid with equal frequency, but parasitized significantly more of the former; both kinds of aphids were attacked and parasitized at higher rates than pink alfalfa aphid. In the dark, P. pequodorum females parasitized green and pink alfalfa aphids equally and at higher rates than pea aphids. Whereas E. californicus was more successful ovipositing in immobilized hosts, P. pequodorum females attacked and laid more eggs in normal than anaesthetized aphids. Patterns of host recognition and evaluation are compared across six species representing four genera in the family Aphidiidae.     

Complex interactions between a plant pathogen and insect parasitoid via the shared vector-host: consequences for host plant infection

Plant viruses modify the development of their aphid vectors by inducing physiological changes in the shared host plant. The performance of hymenopterous parasitoids exploiting these aphids can also be modified by the presence of the plant pathogen. We used laboratory and glasshouse microcosms containing beans (Vicia faba) as the host plant to examine the interactions between a plant virus (pea enation mosaic virus; PEMV) and a hymenopterous parasitoid (Aphidius ervi) that share the aphid vector/host Acyrthosiphon pisum. Neither PEMV-infection of V. faba, nor the carriage of PEMV virions by A. pisum, affected the growth or morphology of the aphid, or the oviposition behaviour and development of A. ervi. The presence of developing Aphidius ervi larvae within Acyrthosiphon pisum did not affect the ability of the aphids to transmit PEMV. However, by reducing their longevity, parasitism ultimately decreased the time viruliferous aphids were able to inoculate plants. In terms of virus dispersal, parasitized aphids exhibited more movement around experimental arenas than unparasitized controls, causing a slight increase in the proportion of beans infected with PEMV. Exposure to adult Aphidius ervi caused Acyrthosiphon pisum to rapidly drop off bean plants and disperse to new hosts, resulting in considerably higher plant infection rates (70%) than that seen in control arenas (25%). The results of this investigation demonstrate that when parasitoids are added to a plant-pathogen-vector system, benefits to the host plant due to reduced herbivore infestation must be balanced against the consequences of parasitoid-induced aphid dispersal and a subsequent increase in the level of plant infection.     

Aphid population dynamics: does resistance to parasitism influence population size?

1. Insect population size is regulated by both intrinsic traits of organisms and extrinsic factors. The impacts of natural enemies are typically considered to be extrinsic factors, however insects have traits that affect their vulnerability to attack by natural enemies, and thus intrinsic and extrinsic factors can interact in their effects on population size. 2. Pea aphids Acyrthosiphon pisum Harris (Hemiptera: Aphididae) in New York and Maryland that are specialised on alfalfa are approximately two times more physiologically resistant to parasitism by Aphidius ervi Haliday (Hymenoptera: Braconidae) than pea aphids specialised on clover. To assess the potential influence of this genetically based difference in resistance to parasitism on pea aphid population dynamics, pea aphids, A. ervi, and other natural enemies of aphids in clover and alfalfa fields were sampled. 3. Rates of successful parasitism by A. ervi were higher and pea aphid population sizes were lower in clover, where the aphids are less resistant to parasitism. In contrast, mortality due to a fungal pathogen of pea aphids was higher in alfalfa. Generalist aphid predators did not differ significantly in density between the crops. 4. To explore whether intrinsic resistance to parasitism influences field dynamics, the relationship between resistance and successful field parasitism in 12 populations was analysed. The average level of resistance of a population strongly predicts rates of successful parasitism in the field. The ability of the parasitoid to regulate the aphid may vary among pea aphid populations of different levels of resistance.     

A facultative mutualism between aphids and an invasive ant increases plant reproduction

1. The consequences to plants of ant–aphid mutualisms, particularly those involving invasive ants, are poorly studied. Ant–aphid mutualisms may increase or decrease plant fitness depending on the relative cost of herbivory by ant‐tended aphids versus the relative benefit of increased ant suppression of other (non‐aphid) herbivores. 2. We conducted field and greenhouse experiments in which we manipulated the presence and absence of cotton aphids (Aphis gossypii) on cotton plants to test the hypothesis that a mutualism between cotton aphids and an invasive ant, the red imported fire ant (Solenopsis invicta), benefits cotton plants by increasing fire ant suppression of caterpillars. We also manipulated caterpillar abundance to test whether the benefit of the mutualism varied with caterpillar density. 3. We found that more fire ants foraged on plants with cotton aphids than on plants without cotton aphids, which resulted in a significant reduction in caterpillar survival and caterpillar herbivory of leaves, flower buds, and bolls on plants with aphids. Consequently, cotton aphids indirectly increased cotton reproduction: plants with cotton aphids produced 16% more bolls, 25% more seeds, and 10% greater seedcotton mass than plants without aphids. The indirect benefit of cotton aphids, however, varied with caterpillar density: the number of bolls per plant at harvest was 32% greater on plants with aphids than on plants without aphids at high caterpillar density, versus just 3% greater at low caterpillar density. 4. Our results highlight the potential benefit to plants that host ant–hemipteran mutualisms and provide the first experimental evidence that the consequences to plants of an ant–aphid mutualism vary at different densities of non‐aphid herbivores.     

Using food for different purposes: female responses to prey in the predator Coccinella septempunctata L. (Coleoptera: Coccinellidae)

Abstract.  1. Although predatory insects often feed on diverse prey, their reproductive activity may be linked most strongly to a more restricted range of prey. The propensity of adult females of the ladybird beetle, Coccinella septempunctata L., to attack two natural prey species, pea aphids [ Acyrthosiphon pisum (Harris)] and alfalfa weevil larvae [ Hypera postica (Gyllenhal)], was compared, and the degree to which ladybird egg production depends on consumption of aphids vs. weevils was assessed.
2. Coccinella septempunctata females more readily attacked aphids than weevil larvae. This was true regardless of whether females had fed previously on aphids or on weevil larvae.
3. When females were provided with few to many aphids daily, or few aphids plus an excess number of weevil larvae, their rates of egg production depended primarily on the number of aphids consumed.
4. Addition of weevil larvae to diets of limited numbers of aphids increased egg production, but only modestly. Thus, consumption of weevil larvae may have served mostly for self-maintenance, thereby enabling females to use for egg production more of the nutrients and energy obtained from limited consumption of aphids.
5. The females' linkage of egg production primarily to aphid rather than weevil consumption may be adaptive, as their offspring are much less able as larvae to survive and mature on a diet of weevils rather than aphids.     

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.