Impact of intraguild predation by adult Harmonia axyridis (Coleoptera: Coccinellidae) on Aphis glycines (Hemiptera: Aphididae) biological control in cage studies

The soybean aphid, Aphis glycines Matsumura, has become a principal arthropod pest of soybean in the U.S. since its first detection in 2000. This species threatens soybean production through direct feeding damage and virus transmission. A diverse guild of insect predators feeds on soybean aphid in Michigan including the exotic coccinellid Harmonia axyridis, the native gall midge Aphidoletes aphidimyza and the native lacewing Chrysoperla carnea. In addition to feeding on A. glycines some members of this guild may also engage in intraguild predation. These interactions may produce positive, negative, or neutral impacts on A. glycines biological control. We explored the impact of intraguild predation on soybean aphid population dynamics by comparing aphid populations in microcosms with either A. aphidimyza larvae or C. carnea larvae alone, with both a H. axyridis adult and either A. aphidimyza or C. carnea larvae, and without predators. When H. axyridis was present with larval A. aphidimyza or C. carnea, the lady beetle acted as an intraguild predator. However, intraguild feeding did not result in a release of aphid populations compared with microcosms containing only the intraguild and aphid prey. A similar result was found in field cages. Cages allowing large predators had reduced numbers of A. aphidimyza and C. carnea larvae but also significantly fewer aphids compared with predator exclusion cages. Thus, in both lab and field studies the direct impact of H. axyridis on A. glycines overcame its negative impact as an intraguild predator. Together, these studies indicate that while the exotic H. axyridis does act as an intraguild predator and may contribute to local declines in A. aphidimyza and C. carnea, it is also currently important in overall biological control of A. glycines.     

Impact of intraguild predation on parasitoid foraging behaviour

1. Trophic interactions between predators and parasitoids can be described as intraguild predation (IGP) and are often asymmetric. Parasitoids (typically the IG prey) may respond to the threat of IGP by mitigating the predation risk for their offspring. 2. We used a system with a facultative predator Macrolophus caliginosus, the parasitoid Aphidius colemani, and their shared prey, the aphid Myzus persicae. We examined the functional responses of the parasitoid in the presence/absence of the predator on two host plants (aubergine and sweet pepper) with differing IGP risk. 3. Estimated model parameters such as parasitoid handling time increased on both plants where the predator was present, but impact of the predator varied with plant species. The predator, which could feed herbivorously on aubergine, had a reduced impact on parasitoid foraging on that plant. IG predator presence could reduce the searching effort of the IG prey depending on the plant, and on likely predation risk. 4. The results are discussed with regard to individual parasitoid's foraging behaviour and population stability; it is suggested that the presence of the predator can contribute to the stabilisation of host–parasitoid dynamics     

Encounters with aphid predators or their residues impede searching and oviposition by the aphid parasitoid Aphidius ervi （Hymenoptera： Aphidiinae）

Intraguild predation （IGP） can be an important factor influencing the effective- ness of aphid natural enemies in biological control. In particular, aphid parasitoid foraging could be influenced by the presence of predators. This study investigated the effect of larvae of the predatory hoverfly Episyrphus balteatus DeGeer （Diptera： Syrphidae） and the multicolored Asian ladybird Harmonia axyridis Pallas （Coleoptera： Coccinellidae） on the foraging behavior of the aphid parasitoid, Aphidius ervi Haliday （Hymenoptera： Aphidiidae） in choice experiments using a leaf disc bioassay. Wasp response to chemical tracks left by those predator larvae was also tested. Parasitoid behavior was recorded using the Observer （Noldus Information Technology, version 5.0, Wageningen, the Netherlands）. The experiments were conducted under controlled environmental conditions using leaves of the broad bean plant, Viciafaba L. （Fabaceae） with Myzus persicae Sulzer （Homoptera： Aphididae） as the host complex. A. ervi females avoided aphid patches when larvae of either predator were present. A similar avoidance response was shown by A. ervi to aphid patches with E. balteatus larval tracks, whereas no significant response was observed to tracks left by H. axyridis larvae. It was concluded that IG predator avoidance shown by the aphid parasitoid A. ervi may be a factor affecting their distribution among host patches.     

Intraguild Predation among the Hoverfly Episyrphus balteatus de Geer (Diptera: Syrphidae) and Other Aphidophagous Predators

Aphidophagous predators compete for the same prey species. During their foraging activity they frequently encounter heterospecific aphid predators. These situations can lead to intraguild predation and may disrupt biological control efforts against aphids where more than one predator species is present. We investigated the behavior of larvae of the hoverfly Episyrphus balteatus de Geer and its interaction with three other aphid predators: the ladybird Coccinella septempunctata L., the lacewing Chrysoperla carnea Stephens, and the gall midge Aphidoletes aphidimyza (Rondani). Interspecific interactions between predators were examined in arenas of different sizes and in the presence of extraguild prey. The outcome of interactions between E. balteatus larvae and the other predators depended predominantly on the relative body size of the competitors. Relatively large individuals acted as intraguild predators, while relatively smaller individuals became intraguild prey. Eggs and first- as well as second-instar larvae of E. balteatus were highly susceptible to predation by all other predators, whereas pupae of E. balteatus were preyed upon only by the larvae of C. carnea. Interactions between A. aphidimyza and E. balteatus were asymmetric and always favored the latter. Eggs and first- as well as second-instar larvae of E. balteatus sustained intraguild predation irrespective of the size of the arena or the presence of extraguild prey. However, the frequency of predation on third-instar larvae of E. balteatus was significantly reduced. This study indicated that the same species can be both intraguild predator and intraguild prey. It is suggested that combinations of predators must be carefully chosen for success in biological control of aphids.     

Avoidance of intraguild predation leads to a long-term positive trait-mediated indirect effect in an insect community

Intraguild predation among natural enemies is common in food webs with insect herbivores at their base. Though intraguild predation may be reciprocal, typically one species suffers more than the other and frequently exhibits behavioural strategies to lessen these effects. How such short-term behaviours influence population dynamics over several generations has been little studied. We worked with a model insect community consisting of two species of aphid feeding on different host plants (Acyrthosiphon pisum on Vicia and Sitobion avenae on Triticum), a parasitoid (Aphidius ervi) that attacks both species, and a dominant intraguild predator (Coccinella septempunctata) that also feeds on both aphids (whether parasitized or not). As reported previously, we found A. ervi avoided chemical traces of C. septempunctata. In population cages in the laboratory, application of C. septempunctata extracts to Vicia plants reduced parasitism on A. pisum. This did not increase parasitism on the other aphid species, our predicted short-term trait-mediated effect. However, a longer term multigenerational consequence of intraguild predator avoidance was observed. In cages where extracts were applied in the first generation of the study, parasitoid recruitment was reduced leading to higher population densities of both aphid species. S. avenae thus benefits from the presence of a dominant intraguild predator foraging on another species of aphid (A. pisum) on a different food plant, a long-term, trait-mediated example of apparent mutualism. The mechanism underlying this effect is hypothesized to be the reduced searching efficiency of a shared parasitoid in the presence of cues associated with the dominant predator.     

The importance of intraguild interactions to the combined effect of a parasitoid and a predator on aphid population suppression

Intraguild predation (IGP) occurs when consumers competing for a resource also engage in predatory interactions. A common type of IGP involves aphid predators and parasitoids: since parasitoid offspring develop within aphid hosts, they are particularly vulnerable to predation by aphid predators such as coccinellid beetles. Other intraguild interactions that include non-lethal behavioral effects, such as interference with foraging and avoidance of IGP, may also hamper parasitoid activity and reduce their effectiveness as biological control agents. In this study, we quantified mortality in and behavioral effects on Aphidius colemani Viereck (Hymenoptera: Aphidiidae) by its IG-predator Coccinella undecimpunctata L. (Coleoptera: Coccinellidae), and compared the impact of two release ratios of these natural enemies on aphid populations. Parasitoids did not leave the plant onto which they were first introduced, regardless of the presence of predators, even when alternative prey was offered on predator-free plants nearby. In 2-hour experiments, predator larvae interfered with wasp activity, and the level of aphid parasitism was lower in the presence of predators than in their absence. In these experiments, the parasitoids contributed more to aphid mortality than the predators and aphid suppression was higher when a parasitoid acted alone than in combination with a predator larva. These results were confirmed in a 5-day experiment, but only at one parasitoid:predator release ratio (4:3) not another (2:3). The over-all impact on aphid population growth was non-the-less stronger when both enemies acted together than when only one of them was present. Results indicate that for given release ratios and time scale, the negative lethal and non-lethal effects of the predator on parasitoid performance did not fully cancelled the direct impact of the predator on the aphid population.     

Density-dependent intraguild predation of an aphid parasitoid

A growing body of research has examined the effect of shared resource density on intraguild predation (IGP) over relatively short time frames. Most of this work has led to the conclusion that when the shared resource density is high, the strength of IGP should be lower, due to prey dilution. However, experiments addressing this topic have been done using micro- or mesocosms that excluded the possibility of intraguild predator aggregation. We examined the effect of shared resource density on IGP of an aphid parasitoid in an open field setting where the effects of prey dilution and predator aggregation could occur simultaneously. We brought potted soybean plants with 2, 20, or 200 soybean aphids (Aphis glycines) and 20 pupae (‘mummies’) of the soybean aphid parasitoid Binodoxys communis into soybean fields in Minnesota, USA. We monitored predator aggregation onto the potted plants, predation of parasitoid mummies, and successful adult emergence of B. communis. We found that predator aggregation was higher at the higher aphid densities on our experimental plants and that this coincided with lower adult emergence of B. communis, indicating that even if a prey dilution effect occurred in our study, it was overcome by short-term predator aggregation. Our results suggest that the effect of shared resource density on IGP may be more nuanced in a field setting than in microcosms due to predator aggregation.     

Predator and parasitoid attacking ant-attended aphids: effects of predator presence and attending ant species on emerging parasitoid numbers

Interaction between a predator and a parasitoid attacking ant-attended aphids was examined in a system on photinia plants, consisting of the aphid Aphis spiraecola, the two ants Lasius japonicus and Pristomyrmex pungens, the predatory ladybird beetle Scymnus posticalis, and the parasitoid wasp Lysiphlebus japonicus. The ladybird larvae are densely covered with waxy secretion and are never attacked by attending ants. The parasitoid females are often attacked by ants, but successfully oviposit by avoiding ants. The two ants differ in aggressiveness towards aphid enemies. Impacts of the predator larvae and attending ant species on the number of parasitoid adults emerging from mummies per aphid colony were assessed by manipulating the presence of the predator in introduced aphid colonies attended by either ant. The experiment showed a significant negative impact of the predator on emerging parasitoid numbers. This is due to consumption of healthy aphids by the predator and its predation on parasitized aphids containing the parasitoid larvae (intraguild predation). Additionally, attending ant species significantly affected emerging parasitoid numbers, with more parasitoids in P. pungens-attended colonies. This results from the lower extent of interference with parasitoid oviposition by the less aggressive P. pungens. Furthermore, the predator reduced emerging parasitoid numbers more when P. pungens attended aphids. This may be ascribed to larger numbers of the predator and the resulting higher levels of predation on unparasitized and parasitized aphids in P. pungens-attended colonies. In conclusion, a negative effect of the predator on the parasitoid occurs in ant-attended aphid colonies, and the intensity of the interaction is affected by ant species.     

Microcosm studies on intraguild predation between female erigonid spiders and lacewing larvae and influence of single versus multiple predators on cereal aphids

Abstract: Intraguild predation between female erigonid spiders [Erigone atra (Blackwall) and Oedothorax apicatus (Blackwall), Araneae, Erigonidae] and lacewing larvae (second instar larvae of Chrysoperla carnea (Stephens), Neuropt., Chrysopidae) and interaction effects of predator combinations on cereal aphids were investigated in a microcosm system under laboratory conditions. The microcosm experiments were run for 7 days and consisted of 15wheat seedlings, 15 Sitobion avenae (F) (Hom., Aphididae) as start population, plus a female spider or a lacewing larva or a combination of a spider plus a lacewing larva. The mortality rate of lacewing larvae was significantly increased by 44 and 31% due to intraguild predation by female spiders of E. atra and O. apicatus in comparison with lacewing larvae that were kept alone. The final aphid numbers in the microcosms were significantly reduced by all single predator treatments (spiders, lacewing larvae) and the predator combinations in comparison with controls without predators. The predation effect on aphid populations due to both spider species was similar and not statistically different. An additive effect of the predator combinations ‘spider plus surviving lacewing larva’ was found for both spider species resulting in reduced aphid numbers compared with the single predator treatments. When the lacewing larva was killed by an E. atra female the effects on aphids were non‐additive, but aphid numbers were not statistically increased compared with the lacewing larva treatment. When the lacewing larva was killed by an O. apicatus female, the effects of spider and C. carnea larva were additive on aphid numbers. In the presence of additional prey (fruit flies and Collembola) intraguild predation was not found and E. atra females had no significant effect on the survival of lacewing larvae. In addition, E. atra females had no significant effect on aphid numbers in the presence of fruit flies and Collembola, but in combination with a lacewing larva that survived, a significantly greater reduction of the aphid population was observed compared with the lacewing larva treatment. The body mass of lacewing larvae at the end of the experiment was not statistically influenced by the presence or absence of an E. atra female.     

Influence of intraguild predation among generalist insect predators on the suppression of an herbivore population

We evaluated the influence of intraguild predation among generalist insect predators on the suppression of an herbivore, the aphid Aphis gossypii, to test the appropriateness of the simple three trophic level model proposed by Hairston, Smith, and Slobodkin (1960). We manipulated components of the predator community, including three hemipteran predators and larvae of the predatory green lacewing Chrysoperla carnea, in field enclosure/exclosure experiments to address four questions: (1) Do generalist hemipteran predators feed on C. carnea? (2) Does intraguild predation (IGP) represent a substantial source of mortality for C. carnea? (3) Do predator species act in an independent, additive manner, or do significant interactions occur? (4) Can the experimental addition of some predators result in increased densities of aphids through a trophic cascade effect? Direct observations of predation in the field demonstrated that several generalist predators consume C. carnea and other carnivorous arthropods. Severely reduced survivorship of lacewing larvae in the presence of other predators showed that IGP was a major source of mortality. Decreased survival of lacewing larvae was primarily a result of predation rather than competition. IGP created significant interactions between the influences of lacewings and either Zelus renardii or Nabis predators on aphid population suppression. Despite the fact that the trophic web was too complex to delineate distinct trophic levels within the predatory arthropod community, some trophic links were sufficiently strong to produce cascades from higher-order carnivores to the level of herbivore population dynamics: experimental addition of either Z. renardii or Nabis predators generated sufficient lacewing larval mortality in one experiment to release aphid populations from regulation by lacewing predators. We conclude that intraguild predation in this system is wide-spread and has potentially important influences on the population dynamics of a key herbivore.     

Use of odours by Cycloneda sanguinea to assess patch quality

Adult ladybirds are likely to encounter various species of prey when foraging for oviposition sites. Optimal oviposition theory predicts that females should lay eggs in those sites that are the most suitable for offspring development. Therefore, factors that directly affect offspring mortality, such as the presence of predators and food, are expected to play an important role in the assessment of patch profitability by ladybird predators. Using a Y‐tube olfactometer, we tested whether the predatory ladybird Cycloneda sanguinea L. (Coleoptera: Coccinellidae) can use volatile cues to assess patch profitability and avoid predator‐rich patches. We assessed the foraging behaviour of C. sanguinea in response to odours associated with tomato plants infested with a superior prey, Macrosiphum euphorbiae Thomas (Homoptera: Aphididae), and with an inferior prey, Tetranychus evansi Baker and Pritchard (Acari: Tetranychidae), in the presence or absence of the heterospecific predator Eriopis connexa Mulsant (Coleoptera: Coccinellidae). Females of C. sanguinea significantly preferred plants infested by M. euphorbiae to plants infested by T. evansi and avoided odours emanating from plants on which E. connexa females were present. Our results show that C. sanguinea use volatile cues to assess patch profitability and to avoid patches with heterospecific competitors or intraguild predators.     

Foraging strategies and patch distributions: intraguild interactions between Dicyphus hesperus and Encarsia formosa

Abstract 1. Competing foragers are affected by the distribution of resources, but can also affect resource distribution. Intraguild predators may affect the distribution of both the shared prey and the intraguild prey, which are also their competitors. 2. Variation in foraging strategies and their effects on resource distributions may influence the outcome of intraguild interactions between an intraguild predator and its intraguild prey. This was tested using whitefly Trialeurodes vaporariorum as the shared resource, the parasitoid Encarsia formosa as the intraguild prey, and Dicyphus hesperus, an omnivore, as the intraguild predator on tomato (Lycopersicon esculentum) and mullein (Verbascum thapsus) plants, within enclosures in a greenhouse. Treatments were established with and without the intraguild predator and at high and low intraguild prey densities. 3. The interaction between D. hesperus and E. formosa showed significant asymmetry, with D. hesperus populations being unaffected by E. formosa densities, although E. formosa populations were reduced by the inclusion of D. hesperus. However, the inclusion of D. hesperus diminished density‐dependent effects limiting E. formosa populations at high release densities. 4. Dicyphus hesperus reduced the average patch size and the proportion of patches occupied by whitefly. Increasing the release rate of E. formosa had no effect on any distributional measure. Based upon the foraging ecology of both species, the foraging activities of D. hesperus appear to have modified the patch distribution so that its foraging strategy becomes more successful than that of E. formosa. These properties may provide an important mechanism determining the outcome of species interactions.     

Behavioural Response of Juvenile Bluegill Sunfish to Variation in Predation Risk and Food Level

The behavioural response of juvenile bluegill sunfish (Lepomis macrochirus) to predation risk when selecting between patches of artificial vegetation differing in food and stem density was investigated. Bluegill foraging activity was significantly affected by all three factors. Regardless of patch stem density or risk of predation bluegills preferred patches with the highest prey number. During each trial bluegill foraging activity was clearly divided into a between- and within-patch component. In the presence of a predator bluegills reduced their between-patch foraging activity by an equivalent amount regardless of patch stem density or food level, apparently showing a risk-adjusting behavioural response to predation risk. Within patches, however, foraging activity was affected by both food level and patch stem density. When foraging in a patch offering a refuge from predation, the presence of a predator had no effect on bluegill foraging activity within this patch. However, if foraging in a patch with only limited refuge potential, bluegill foraging activity was reduced significantly in the presence of a predator. Further, this reduction was significantly greater if the patch contained a low versus a high food level, indicating a risk-balancing response to predation with respect to within-patch foraging activity. Both these responses differ from the risk-avoidance response to predation demonstrated by juvenile bluegills when selecting among habitats. Therefore, our results demonstrate the flexibility of juvenile bluegill foraging behaviour.     

Potential for biotic interference of a classical biological control agent of the soybean aphid

The degree to which resident biota can inhibit the ability of an introduced biological control agent to establish and be effective is termed biotic interference. Studying biotic interference prior to a release using the actual agent is logistically difficult, however, due to quarantine restrictions. An alternative solution is to study biotic interference against a surrogate species in the intended range of introduction, with the expectation that biotic interference against the actual agent will be similar. This study assessed how biotic interference, mostly by generalist predators, may affect establishment of classical biological control agents of the soybean aphid, Aphis glycines Matsumura, in North America. The parasitoid Aphidius colemani Viereck was used as a surrogate for Asian aphidiine braconids such as Binodoxys communis (Gahan). We conducted a factorial field experiment that measured the effect of releasing A. colemani and of excluding resident natural enemies using field cages on soybean aphid populations. We also conducted molecular gut-contents analyses on predators collected in release plots to determine which species fed upon A. colemani. Releasing A. colemani in open field plots increased soybean aphid control beyond that observed in open field plots alone, despite indications that intraguild predation of A. colemani occurred. Thus, biotic interference was not sufficient to eliminate the contribution of A. colemani on soybean aphid suppression during the course of our experiment. Molecular gut-contents analysis revealed that at least two predators, Harmonia axyridis (Pallas) and Chrysoperla carnea Stephens, engaged in intraguild predation against A. colemani. The prolonged effect of intraguild predation on parasitoid establishment remains to be determined.     

Long handling times of Praon unicum by Harmonia axyridis result in protection from predation

The intraguild predator Harmonia axyridis has a longer handling time of Praon unicum mummies in contrast to Aphidius matricariae mummies and the pest aphid Myzus persicae. In addition, the rejection rate of P. unicum is higher as compared to the A. matricariae and M. persicae. Harmonia Axyridis also has a shorter residence times when foraging in P. unicum patches. The longer handling time may provide P. unicum with a refuge from intraguild predation by H. axyridis. Thus, Praon unicum could be a better biocontrol agent than A. matricariae in the presence of intraguild predation, as it will face lower predation rates.     

Intraguild Interactions Between the Predatory Mites Neoseiulus californicus and Phytoseiulus persimilis

Species at the same trophic level may interact through competition for food, but can also interact through intraguild predation. Intraguild predation is widespread at the second and third trophic level and the effects may cascade down to the plant level. The effects of intraguild predation can be modified by antipredator behaviour in the intraguild prey. We studied intraguild predation and antipredator behaviour in two species of predatory mite, Neoseiulus californicus and Phytoseiulus persimilis, which are both used for control of the two-spotted spider mite in greenhouse and outdoor crops. Using a Y-tube olfactometer, we assessed in particular whether each of the two predators avoids odours emanating from prey patches occupied by the heterospecific predator. Furthermore, we measured the occurrence and rate of intraguild predation of different developmental stages of P. persimilis and N. californicus on bean leaves in absence or in presence of the shared prey. Neither of the two predator species avoided prey patches with the heterospecific competitor, both when inexperienced with the other predator and when experienced with prey patches occupied by the heterospecific predator. Intraguild experiments showed that N. californicus is a potential intraguild predator of P. persimilis. However, P. persimilis did not suffer much from intraguild predation as long as the shared prey was present. This is probably because N. californicus prefers to feed on two-spotted spider mites rather than on its intraguild prey.     

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.     

Intraguild Predation by Anthocoris nemorum (Heteroptera: Anthocoridae) on the Aphid Parasitoid Aphidius colemani (Hymenoptera: Braconidae)

The magnitude of intraguild predation by adult females of the predator Anthocoris nemorum on immature larvae of the aphid parasitoid Aphidius colemani inside mummies of peach-potato aphids Myzus persicae was investigated under laboratory conditions in a preference experiment. Each predator consumed a mean (95% confidence limits) of 2.8 (2.1; 3.8) immature parasitoids within mummies and 3.6 (2.7; 4.6) unparasitised aphid nymphs. Thereby A. nemorum engaged in intraguild predation with A. colemani and did not exhibit prey preference between mummies and unparasitised aphids.     

Direct and indirect top‐down effects of previous contact with an enemy on the feeding behavior of blowfly larvae

We investigated the addition of a trophic level to a simple food web. Direct and indirect effects caused by the presence of a new species in the food web were quantified by estimating survival and consumption rates on the basal resource. We focused on a blowfly intraguild prey–predator system with various ecological interactions taking place during the larval period. The experiments were designed to set Chrysomya megacephala (Fabricius) (Diptera: Calliphoridae) as the intraguild prey and Chrysomya albiceps (Wiedemann) as the intraguild predator and/or cannibal. The generalist pupal parasitoid Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) was introduced into the system during a non‐susceptible life stage of the interacting blowfly species. The cascading parasitoid effects induced behavioral changes in the blowfly larvae, increasing the impact of intraguild predation and cannibalism on blowfly survival. The results suggest that blowfly larvae can change their feeding behavior in response to the presence of a parasitoid.     

Oviposition avoidance of parasitized aphid colonies by the syrphid predator Episyrphus balteatus mediated by different cues

Oviposition decisions made by members of a guild of natural enemies can have evolved to avoid intraguild predation, potentially avoiding the disruption of the extraguild prey control. We have studied the oviposition preference of the aphidophagous predator Episyrphus balteatus De Geer (Diptera: Syrphidae) within colonies of Myzus persicae Sulzer (Hemiptera: Aphididae) in the presence of two developmental stages of the aphid parasitoid Aphidius colemani Viereck (Hymenoptera: Aphidiidae). Results from a greenhouse choice experiment showed that E. balteatus females lay significantly fewer eggs in colonies with mummified aphids than in unparasitized colonies. Colonies of parasitized, but not yet mummified did not contain significantly fewer eggs than colonies with unparasitized aphids. In three no-choice experiments, we assessed stimuli coming from aphid honeydew, from the aphids themselves and also from extracts of the aphid bodies, and all of these stimuli mediate the discrimination of mummified aphids from healthy aphids. To a lesser extent these stimuli also contribute to the discrimination against aphids that are parasitized but not yet mummified. These results suggest that the effects of these two species could be complementary for the control of M. persicae, since the species that acts as an intraguild predator, E. balteatus, avoids ovipositing on aphid colonies parasitized by the intraguild prey, A. colemani.