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.     

Functional responses of aphid parasitoids,Aphidius colemani (Hymenoptera: Braconidae) and Aphelinus asychis (Hymenoptera: Aphelinidae)

We evaluated the functional responses of two aphid parasitoids: Aphidius colemani on the green peach aphid Myzus persicae (Hemiptera: Aphididae), and Aphelinus asychis on M. persicae and the potato aphid, Macrosiphum euphorbiae (Hemiptera: Aphididae). Parasitoid oviposition occurred at host densities of 5, 10, 20, 30, 50, 80 or 100 aphids for A. colemani and 5, 10, 20, 30 or 50 aphids for A. asychis. More M. persicae were parasitized by A. colemani than by A. asychis at an aphid density of 50. Among the three types of functional response, type III best described the parasitoid response to the host densities both in A. colemani and A. asychis. The estimated handling time was shorter for A. colemani than for A. asychis (0.017 and 0.043 d, respectively). The proportion of aphids that were parasitized exhibited the same characteristic curve among the three host-parasitoid combinations: a wave form that appeared to be a composite of a decelerating (as in type II) response at low host density and an accelerating-and-decelerating (as in type III) response at medium to high host density. We hypothesize that the novel host species (and its host plant), density-dependent superparasitism, and/or density-dependent host-killing may have induced the modified type III response.     

Oviposition vs. offspring fitness in Aphidius colemani parasitizing different aphid species

We measured the acceptance and suitability of four aphid species [Aphis gossypii Glover, Myzus persicae (Sulzer), Rhopalosiphum padi (L.), and Schizaphis graminum (Rondani)] (Homoptera: Aphididae) for the parasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae). Female parasitoids parasitized fewer R. padi than the other three aphid species, and fewer offspring successfully completed development in R. padi than in the other three host species. Sex ratios of emerging adults were more male‐biased from R. padi than from the other three aphid species, suggesting that R. padi is a poor quality host for this population of A. colemani. Ovipositing A. colemani encountered R. padi at a slower rate, spent more time handling R. padi, and parasitoid offspring died at a higher rate in R. padi compared to A. gossypii. Our results show that oviposition behavior and offspring performance are correlated. In each experiment, we tested the effect of the host species in which the parasitoids developed (parental host) on the number of hosts attacked, the proportion of each host species accepted for oviposition and the survival of progeny. Parental host affected maternal body size and, through its effect on body size, the rate of encounter with hosts. Other than this, parental host species did not affect parasitism.     

Foraging patterns of two aphid parasitoids, Lysiphlebus testaceipes and Aphidius colemani on banana

The searching behaviour of two aphid parasitoids, Lysiphlebus testaceipes (Cresson) and Aphidius colemani Viereck (Hymenoptera, Aphidiidae), was analysed. Both species searched banana plants (Musa spec.) infested with the banana aphid Pentalonia nigronervosa Coq. in a different way. L. testaceipes restricted its search to open plant structures and avoided concealed areas. A. colemani partitioned its time spent on the plant between open and concealed areas. This general pattern was independent of aphid colony size and was also observed in the absence of aphids. As a consequence of these searching tactics, the borders of a host patch differed for both parasitoid species. For L. testaceipes, the patch consisted only of aphids feeding on open structures, while it comprised the whole aphid colony for A. colemani. The observed searching patterns resulted in a different exploitation of the aphid colonies.

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Zusammenfassung Eine Analyse des Suchverhaltens der beiden Blattlausparasitoide Lysiphlebus testaceipes (Cresson) and Aphidius colemani Viereck zeigte, daß beide Arten Bananenpflanzen (Musa spec.), die von der Bananenblattlaus Pentalonia nigronervosa Coq. befallen waren, auf unterschiedliche Weise absuchten. L. testaceipes beschränkte seine Wirtssuche auf frei zugängliche Pflanzenteile und vermied ein Eindringen in geschützte Pflanzenstruckturen. Dagegen hielt sich A. colemani gleichermaßen häufig auf offenen und in geschützten Pflanzenteilen auf. Dieses generelle Suchmuster war unabängig von der Blattlauskoloniegröß und wurde auch beim Fehlen von Wirten beobachtet. Als Konsequenz aus diesem unterschiedlichen Suchverhalten ergaben sich verschiedene Patchgrenzen für beide Parasitoide. Für L. testaceipes bestand der Patch nur aus Blattläusen, die an frei zugänglichen Pflanzenstrukturen saugten, während der Patch für A. colemani alle Blattläuse einschließlich der Tiere umfaßte, die sich in geschützten Pflanzenteilen aufhielten. Damit führte dieses unterschiedliche Suchverhalten beider Parasitoidenarten zu einer unterschiedlichen Ausnutzung der Blattlauskolonien.

     

Specialisation of bacterial endosymbionts that protect aphids from parasitoids

1. Infection by the bacterial endosymbiont Hamiltonella defensa is capable of protecting the pea aphid from parasitism by Aphidius ervi and the black bean aphid from parasitism by Lysiphlebus fabarum. Here we investigate protection of a third aphid species, the cowpea aphid, Aphis craccivora, from four parasitoid species: Binodoxys communis, B. koreanus, Lysiphlebus orientalis, and Aphidius colemani. 2. We compared parasitism of A. craccivora lines that were either infected with, or cured of H. defensa separately for the four parasitoid species. Infection by H. defensa almost completely eliminated parasitism of A. craccivora by B. communis and B. koreanus, but had no effect on parasitism by L. orientalis and A. colemani. 3. This indicates at least genus‐level specificity of protective effects by H. defensa and we discuss implications of our findings on the known world‐wide distribution of this host/symbiont interaction.     

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.     

Evaluation of four aphidiine parasitoids for biological control ofAphis gossypii

Four aphidiine parasitoid species (Hymenoptera: Braconidae) were evaluated with respect to their potential to controlAphis gossypii Glover (Homoptera: Aphididae) in glasshouse cucumbers. In a laboratory experiment thirty cotton aphids were offered to individual females for two hours.Aphidius matricariae Haliday parasitized less than six percent of the aphids and was ruled out as potential biological control agent.Ephedrus cerasicola Stary andLysiphlebus testaceipes Cresson parasitized 23 and 26 percent of the aphids, respectively.Aphidius colemani Viereck parasitized 72 to 80 percent of the aphids. With the latter three species, experiments were performed in small glasshouses with cucumbers (Cucumis sativus L. cv. ‘Aramon’). As in the laboratory testA. colemani performed best; significantly more colonies were found and parasitization rates in the colonies were higher byA. colemani than byE. cerasicola andL. testaceipes. Because of the good correspondence between laboratory and glasshouse experiments, it is suggested that bad performance of an aphid parasitoid species in a simple laboratory trial might be sufficient evidence to disregard this species for further tests.     

Ecology of the aphid pests of protected pepper crops and their parasitoids

Myzus persicae, Macrosiphum euphorbiae, Aphis gossypii and Aulacorthum solani (Homoptera: Aphididae) are principal pests of protected pepper crops in southeastern Spain. Our goal was to determine the incidence of aphids on pepper crops and the role of vegetation surrounding greenhouses as a source of aphids and their parasitoids. The population dynamics were followed in six commercial greenhouses during 3 years. Another 82 greenhouses and their surrounding vegetation were surveyed occasionally. Myzus persicae had the highest incidence in pepper greenhouses followed by M. euphorbiae and A. solani. Parasitism of all aphid species in greenhouses was low, Aphidius matricariae and Aphidius colemani being the most abundant parasitoids. Myzus persicae and Macrosiphum euphorbiae were the most abundant and polyphagous aphids, being present on 77 and 55% of the plants sampled outside greenhouses, respectively; species of Brassicaceae were the main hosts for both aphids. Aulacorthum solani was only present on Malva parviflora and at low numbers. Outside greenhouses, A. matricariae was the most common parasitoid of M. persicae, followed by Diaeretiella rapae and A. colemani. Aphidius matricariae was the most polyphagous, being present in 10 out of 22 aphid species. Macrosiphum euphorbiae and A. solani were both parasitised by A. ervi and Praon volucre. Aphelinus asychis was found on A. solani. Parasitoids were found in other aphids not attacking pepper. The role of natural vegetation as a reservoir of aphid pests of pepper and of parasitoids is discussed.     

Floral resources to enhance the potential of the parasitoid Aphidius colemani for biological control of the aphid Myzus persicae

Flowering plants have been widely used to enhance biological control. However, this approach has been limited to some extent by the lack of suitable flowering plant species of wide applicability, particularly for global pests. A key example is the green peach aphid, Myzus persicae (GPA). It is commonly attacked by the polyphagous koinobiont aphidiidae, Aphidius colemani, which is also of global occurrence. Here, eight flowering plants were evaluated for the potential enhancement of GPA biological control using A. colemani under laboratory conditions. These included buckwheat (Fagopyrum esculentum), alyssum (Lobularia maritima), white rocket (Diplotaxis erucoides.), wild mustard (Sinapis arvensis), lavender (Lavandula angustifolia), wild marjoram (Origanum vulgare), thyme (Origanum marjorana) and pepper mint (Mentha piperita). The effects of access to these flowers on the longevity (days), potential fecundity (number of dissected eggs) and parasitism rate for A. colemani compared with the control treatment (water) were studied. Longevity of A. colemani which had access to buckwheat was 4–5 times longer than the control and 2–3 times longer than it was in the other plant treatments; the latter did not differ significantly between each other. Potential fecundity of A. colemani was the highest when it had been provided with buckwheat flowers. Exposing A. colemani to flowering plants for longer time intervals (12 hr and 24 hr) increased the number of eggs produced compared with 6 hr. The number of parasitized aphids/female A. colemani with buckwheat flowers was the highest of all treatments; it ranged from 14 in the control to 219 with buckwheat. Further studies should be carried out under field conditions to determine the effect of a range of flowering plants on A. colemani. For example, although buckwheat was highly effective, in many climates it may be a useful component in mixtures comprising other, more robust species.     

Host-range study about four aphid parasitoid species among 16 aphid species for constructing banker–plant systems

To provide fundamental information for the biological control of aphids in vegetable greenhouses, we compared the host ranges of four aphid parasitoid species, Aphidius colemani Viereck, Aphidius gifuensis Ashmead, Diaeretiella rapae (M’Intosh), and Ephedrus nacheri Quilis (Hymenoptera: Braconidae: Aphidiinae). The acceptability as host of 11 vegetable-pest aphids, Acyrthosiphon pisum (Harris), Aphis craccivora Koch, Aphis gossypii Glover, Aulacorthum solani (Kaltenbach), Brevicoryne brassicae (Linnaeus), Chaetosiphon fragaefolii (Cockerell), Lipaphis erysimi (Kaltenbach), Macrosiphoniella sanborni (Gillette), Macrosiphum euphorbiae (Thomas), Myzus persicae (Sulzer), and Uroleucon formosanum (Takahashi), in addition to five aphid species, Melanaphis sacchari (Zehntner), Rhopalosiphum maidis (Fitch), Rhopalosiphum padi (Linnaeus), Schizaphis graminum (Rondani), and Sitobion akebiae (Shinji) (Hemiptera: Aphididae) that serve as alternative hosts in banker–plant systems for the four aphid parasitoid species, were investigated. A newly emerged pair of parasitoid adults were provided to 100 aphids of each species on caged host plants in a 25 °C chamber for 24 h. The numbers of mummified aphids and emerged adults were counted in 10 trials for each aphid species. Aphidius colemani, A. gifuensis, D. rapae and E. nacheri parasitized four, two, three, and eight pest species, respectively, and four, three, three, and five alternative host species, respectively. Ephedrus nacheri had the broadest host range among the four species, and all the four species parasitized M. persicae, R. maidis, and S. graminum. This information will be useful for selecting candidate of biological control agents for aphids and for constructing banker–plant systems.

     

Compatibility of aphid resistance in soybean and biological control by the parasitoid Aphidius colemani (Hymenoptera: Braconidae)

Biological control and soybean cultivars bred for increased resistance to the soybean aphid (Aphis glycines) are two approaches used to manage this serious pest of soybeans in North America. However, as with many other pest systems, the compatibility of these two pest management approaches has not been studied in detail. The aphidiine wasp Aphidius colemani is one of several candidate species for biological control of the soybean aphid in soybean in North America. Resistance to the soybean aphid in the USDA soybean cultivar Dowling is largely controlled by a single dominant gene Rag1, which is the focus of plant breeding programs directed against the soybean aphid. In this study, we measured developmental and behavioral differences in the parasitic wasp A. colemani when it attacked soybean aphids feeding on either the aphid-resistant Dowling or aphid-susceptible Glenwood cultivars of soybean. We used a combination of choice and no-choice experiments to examine the effects of host plant cultivar on the number of parasitized aphids formed and the sex ratio and body weights of adult offspring produced. Significantly more aphids were parasitized when they fed on Glenwood compared to Dowling and these offspring were larger when they developed in aphids that fed on Glenwood soybeans. To distinguish between effects on foraging decisions and offspring survivorship, we conducted an additional experiment that followed the oviposition decisions and fate of each parasitized aphid. Foraging female A. colemani spent less time handling individual aphids and encountered and attacked aphids at a higher rate when they fed on aphids feeding on Glenwood soybeans than aphids feeding on Dowling soybeans. Furthermore, wasp survivorship in aphids was greater on Glenwood than Dowling. Taken together, aphid-resistance in soybeans has negative effects on foraging behavior and offspring fitness of A. colemani raising concerns about the compatibility of these two pest management approaches.     

Symbiont‐conferred protection against Hymenopteran parasitoids in aphids: how general is it?

1. Hosts are often targeted by multiple species of parasites, leading to a confluence of selective pressures on them. In response, hosts may either evolve defences that act very generally, or specific defences against particular parasites. Aphids are attacked by multiple species of endoparasitoid wasps, and there is clear evidence that heritable endosymbionts can confer resistance against some of these wasps. Less clear is how symbiont‐conferred resistance in a single host acts against multiple parasitoid species. 2. This question was addressed in the black bean aphid, Aphis fabae (Scopoli). Unprotected aphids and aphids protected by three different strains of the defensive endosymbiont Hamiltonella defensa were exposed to four species of parasitic wasps: the parthenogenetic species Lysiphlebus fabarum (Marshall), which was represented by three different asexual lines, and the sexual species Aphidius colemani (Viereck), Binodoxys angelicae (Halliday), and Aphelinus chaonia (Walker). 3. Hamiltonella defensa provided strong protection against L. fabarum and Aphidius colemani, but there was no evidence that H. defensa‐infected aphids were more resistant to the other parasitoid species. While Aphidius colemani was virtually unable to parasitise any aphids harbouring H. defensa, there was variation among the three asexual lines of L. fabarum in how susceptible they were to the defence provided by the different symbiont strains, resulting in a significant genotype‐by‐genotype interaction. 4. The present results suggest that symbiosis with H. defensa does not provide aphids with a general defence against parasitoid wasps, possibly because some species have evolved specific counter adaptations or because biological differences preclude the symbiont's effectiveness against these species.     

Effect of synthetic and plant‐extracted aphid pheromones on the behaviour of Aphidius colemani

Parasitoid females use several chemical cues to locate hosts. A better knowledge of how they respond to a complex of these cues in a small range may help us to understand how to manipulate the parasitoids in the field. Here, the response of the aphid parasitoid Aphidius colemani to a mixture of odours of synthetic and plant‐extracted nepetalactone (a component of aphid sex pheromone) and to (E)‐β‐farnesene (aphid alarm pheromone) was investigated. The behavioural responses of A. colemani to three semiochemical groups with different concentrations were studied in a square arena. Parasitoid females were significantly attracted by the semiochemicals, when their concentrations were high, in which case the females spent more time in squares with semiochemicals. The majority of females preferred plant‐extracted nepetalactone, when it was in high concentration, but they consistently did not respond to (E)‐β‐farnesene.     

The role of plant chemical cues in determining host preference in the generalist aphid parasitoid Aphidius colemani

The host preference behaviour of the generalist aphid parasitoid Aphidius colemaniwas investigated using a Y-tube olfactometer. Female A. colemanishowed a preference for the host-plant complex on which they had been reared, even though the same aphid host was involved, demonstrating a host plant preference. This preference was not evident when the parasitoids were dissected from their mummies prior to adult emergence. Host plant preference exhibited during host selection appeared to be induced by chemical cues encountered on the mummy case at the time of emergence, but preferences could be changed by subsequent foraging experiences. It is concluded that plant chemical cues play a major role in determining initial preferences through a process of emergence conditioning but that learning processes, involving cues encountered during oviposition in or contact with the host, can modify these initial preferences.     

Effect of Invasive Species of Herbaceous Plants and Associated Aphids (Hemiptera,Sternorrhyncha: Aphididae) on the Structure of Ant Assemblages (Hymenoptera,Formicidae)

—In 2015–2017, attendance of 15 invasive and 22 native species of herbaceous plants by ants was studied in 6 habitats in the environs of Kyiv (Ukraine). Altogether, 14 ant species were found, of which 12 were recorded on invasive plants and 9 on native plants; 8 aphid species were found on 8 invasive plant species. Five invasive plant species (Asclepias syriaca, Heracleum mantegazzianum, Oenothera biennis, Onopordum acanthium, and Amaranthus retroflexus) were found to be attractive to ants, with over a half of all the ant workers in all the habitats being recorded on them; besides, numerous colonies of 7 aphid species were also found on these plants. These invasive plants positively affect the structure of ant assemblages since the aphid colonies provide ants with food resource. The remaining 10 invasive plant species, including 5 transformer species, were poorly visited by ants and housed no aphid colonies, with the exception of Conyza canadensis on which the non-myrmecophilous aphid Uroleucon erigeronense (Thomas, 1878) was found. Two thirds of invasive plant species had a negative effect on the structure of ant assemblages because they replaced the native plants and thus reduced the trophic resources of aphids.

     

Patch residence decisions made by Aphidius colemani in the presence of a facultative predator

One of the key questions in ecology is how animals optimally allocate their time in an environment with patchily distributed resources and competing organisms. Here we investigate the effects that an aphid predator, Macrolophus caliginosus (Wagner) (Hemiptera: Miridae), has on the searching behavior and the patch residence decisions of an aphid parasitoid, Aphidius colemani (Viereck) (Hymenoptera: Aphidiidae). A computer programme was designed that allowed the recording and saving of direct observations. The time allocated to different activities by a female parasitoid wasp in the presence or absence of the predator M. caliginosus was investigated. The experiments were conducted under controlled environment conditions using leaves of sweet pepper, Capsicum annuum L. (Solanaceae) and Myzus persicae (Sulzer) (Hemiptera: Aphididae) as the host plant–prey species system. The parasitoid spent significantly less time on ‘secondary’ activities, such as preening and resting, when the predator was present. Survival analysis showed that the parasitoid had a higher patch-leaving tendency when the predator was present.     

Optimal foraging by an aphid parasitoid affects the outcome of apparent competition

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Inoculation of susceptible and resistant potato plants with the late blight pathogen Phytophthora infestans: effects on an aphid and its parasitoid

Plants are exposed to microbial pathogens as well as herbivorous insects and their natural enemies. Here, we examined the effects of inoculation of potato plants, Solanum tuberosum L. (Solanaceae), with the late blight pathogen Phytophthora infestans (Mont.) de Bary (Peronosporales: Pythiaceae) on an aphid species commonly infesting potato crops and one of the aphid's major parasitoids. We observed the peach‐potato aphid, Myzus persicae Sulzer (Hemiptera: Aphididae), and its natural enemy, the biocontrol agent Aphidius colemani Viereck (Hymenoptera: Braconidae), on potato either inoculated with water or P. infestans. Population growth of the aphid, parasitism rate of its natural enemy, and other insect life‐history traits were compared on several potato genotypes, the susceptible cultivar Désirée and genetically modified (GM) isogenic lines carrying genes conferring resistance to P. infestans. Effects of P. infestans inoculation on the intrinsic rate of aphid population increase and the performance of the parasitoid were only found on the susceptible cultivar. Insect traits were similar when comparing inoculated with non‐inoculated resistant GM genotypes. We also tested how GM‐plant characteristics such as location of gene insertion and number of R genes could influence non‐target insects by comparing insect performance among GM events. Different transformation events leading to different positions of R‐gene insertion in the genome influenced aphids either with or without P. infestans infection, whereas effects of position of R‐gene insertion on the parasitoid A. colemani were evident only in the presence of inoculation with P. infestans. We conclude that it is important to study different transformation events before continuing with further stages of risk assessment of this GM crop. This provides important information on the effects of plant resistance to a phytopathogen on non‐target insects at various trophic levels.     

Potential exposure of a classical biological control agent of the soybean aphid, Aphis glycines, on non-target aphids in North America

In summer 2007, the Asian parasitoid Binodoxys communis (Hymenoptera: Braconidae) was released in North America for control of the exotic soybean aphid, Aphis glycines (Hemiptera: Aphididae). Despite its comparatively narrow host range, releases of B. communis may still constitute a risk to native aphid species. To estimate the risk of exposure of non-target aphids to B. communis, we merged assessments of temporal co-occurrence with projections of spatial overlap between B. communis and three native aphid species, and in-field measurements of the incidence of ecological filters that may protect these aphids from parasitism. Temporal co-occurrence was assessed between A. glycines and native aphids (Aphis asclepiadis, Aphis oestlundi, and Aphis monardae) at four different locations in Minnesota, USA. The degree of temporal overlap depended greatly on location and aphid species, ranging between 0 and 100%. All of the native aphids were tended by multiple species of ants, with overall ant-attendance ranging from 26.1 to 89.6%. During temporal overlap with A. glycines, 53 ± 11% of A. monardae colonies were partly found in flower heads of their host plant, with flowers acting as a physical refuge for this aphid. The extent of geographic overlap between B. communis and native aphids based upon Climex modeling was 17–28% for A. monardae, 13–22% for A. oestlundi, 46–55% for A. asclepiadis and 12–24% for the A. asclepiadis species complex. The estimated overall probability of potential exposure of B. communis on native aphids was relatively low (P = 0.115) for A. oestlundi and high (P = 0.550) for A. asclepiades. Physical and ant-mediated refuges considerably lowered probability of population-level impact on A. monardae, and could lead to substantial reduction of exposure for the other native aphids. These findings are used to make broader statements regarding the ecological safety of current B. communis releases and their potential impact on native aphid species in North America.