Application of DNA barcoding to the identification of Hymenoptera parasitoids from the soybean aphid (Aphis glycines) in China

Aphis glycines Matsumura is an important pest of soybean in Asia and North America. Hymenoptera parasitoids play a key role in the control of the soybean aphid. The correct identification of parasitoids is a critical step that precedes the assessment of their potential biological control agents. Accurate identification of the majority of the species attacking the soybean aphid often requires elaborate specimen preparation and expert taxonomic knowledge. In this study, we facilitated the identification of soybean aphid parasitoids by applying a DNA barcoding approach following a preliminary morphological identification. We generated DNA sequence data from the mitochondrial COI gene and the D2 region of 28S rDNA to assess the genetic variation within and between parasitoid species emerging from the soybean aphid in China. Fifteen Hymenoptera parasitoid species belonging to 10 genera of five families were identified with little intra‐specific variation (0.09% ± 0.06% for 28S and 0.36% ± 0.18% for COI) and large inter‐specific divergence (30.46% ± 3.42% for 28S and 20.4% ± 1.20% for COI).     

Large‐scale migration synchrony between parasitoids and their host

1. Parasitoids are a valuable group for conservation biological control. In their role as regulators of aphid pests, it is critical that their lifecycle is synchronised with their hosts in both space and time. This is because a synchronised parasitoid community is more likely to strengthen the overall conservation biological control effect, thus damping aphid numbers and preventing potential outbreaks. One component of this host–parasitoid system was examined, that of migration, and the hypothesis that peak summer parasitoid and host migrations are synchronised in time was tested. 2. Sitobion avenae Fabricius and six associated parasitoids were sampled from 1976 to 2013 using 12.2‐m suction‐traps from two sites in Southern England. The relationship between peak weekly S. avenae counts and their parasitoids was quantified. 3. Simple regression models showed that the response of the peak parasitoids to the host was positive: generally, more parasitoids migrated with increasing numbers of aphids. Further, when averaged over time, the parasitoid migration peak date corresponded with the aphid migration peak. The co‐occurrence of the peaks was between 51% and 64%. However, the summer peak in aphid migration is not steadily shifting forward with time unlike spring first flights of aphids. Cross‐correlation analysis showed that there were no between‐year lagged effects of aphids on parasitoids. 4. These results demonstrate that the peak in migration phenology between host and parasitoid is broadly synchronised within a season. Because the threshold temperature for flight (> 12 °C) was almost always exceeded in summer, the synchronising agent is likely to be crop senescence, not temperature. Studies are needed to assess the effects of climate change on the mismatch potential between parasitoids and their hosts.     

Food web structure of aphids and their parasitoids in Belgian fruit agroecosystems

Community structures of aphids and their parasitoids were studied in fruit crop habitats of eastern Belgium in 2014 and 2015. Quantitative food webs of these insects were constructed separately for each year, and divided into subwebs on three host‐plant categories, fruit crop plants, non‐crop woody and shrub plants and non‐crop herbaceous plants. The webs were analyzed using the standard food web statistics designed for binary data. During the whole study period, 78 plant species were recorded as host plants of 71 aphid species, from which 48 parasitoid species emerged. The community structure, aphid / parasitoid species‐richness ratio and trophic link number varied between the two years, whereas the realized connectance between parasitoids and aphids was relatively constant. A new plant–aphid–parasitoid association for Europe was recorded. Dominant parasitoid species in the study sites were Ephedrus persicae, Binodoxys angelicae and Praon volucre: the first species was frequently observed on non‐crop trees and shrubs, but the other two on non‐crop herbaceous plants. The potential influence, through indirect interactions, of parasitoids on aphid communities was assessed with quantitative parasitoid‐overlap diagrams. Symmetrical links were uncommon, and abundant aphid species seemed to have large indirect effects on less abundant species. These results show that trophic indirect interactions through parasitoids may govern aphid populations in fruit crop habitats with various non‐crop plants, implying the importance for landscape management and biological control of aphid pests in fruit agroecosystems.     

Biological control of the diamondback moth, Plutella xylostella: A review

The diamondback moth (DBM), Plutella xylostella (L.) (Lepidoptera: Plutellidae), is one of the most destructive cosmopolitan insect pests of brassicaceous crops. It was the first crop insect reported to be resistant to DDT and now, in many crucifer producing regions, it has shown significant resistance to almost every synthetic insecticide applied in the field. In certain parts of the world, economical production of crucifers has become almost impossible due to insecticidal control failures. Consequently, increased efforts worldwide have been undertaken to develop integrated pest management (IPM) programs, principally based on manipulation of its natural enemies. Although over 130 parasitoid species are known to attack various life stages of DBM, most control worldwide is achieved by relatively few hymenopteran species belonging to the ichneumonid genera Diadegma and Diadromus, the braconid genera Microplitis and Cotesia, and the eulophid genus Oomyzus. DBM populations native to different regions have genetic and biological differences, and specific parasitoid strains may be associated with the specific DBM strains. Therefore, accurate identification based on genetic studies of both host and parasitoid is of crucial importance to attaining successful control of DBM through inoculative or inundative releases. Although parasitoids of DBM larvae and pupae are currently its principal regulators, bacteria-derived products (e.g., crystal toxins from Bacillus thuringiensis) and myco-insecticides principally based on Zoophthora radicans and Beauveria bassiana are increasingly being applied or investigated for biological control. Viruses, nematodes and microsporidia also have potential as biopesticides for DBM. When an insect pest is exposed to more than one mortality factor, there is the possibility of interactions that can enhance, limit, or limit and enhance the various aspects of effectiveness of a particular control tactic. This paper reviews the effectiveness of various parasitoids and entomopathogens against DBM, interactions among them, and their possible integration into modern IPM programs.     

Strong parasitoid-mediated selection in experimental populations of aphids

Clonal diversity in asexual populations may be maintained if different clones are favoured under different environmental conditions. For aphids, parasitoids are an important variable of the biotic environment. To test whether parasitoids can mediate selection among host clones, we used experimental populations consisting of 10 clones of the peach-potato aphid, Myzus persicae, and allowed them to evolve for several generations either without parasitoids or in the presence of two species of parasitoid wasps. In the absence of parasitoids, strong shifts in clonal frequencies occurred, mostly in favour of clones with high rates of increase. The parasitoid Diaeretiella rapae hardly affected aphid densities but changed the outcome of competition by favouring one entirely resistant clone and disfavouring a highly susceptible clone. Aphidius colemani, the more infective parasitoid, strongly reduced aphid densities and dramatically changed host clonal frequencies. The most resistant clone, not a successful clone without parasitoids, became totally dominant. These results highlight the potential of temporal or spatial variation in parasitoid densities to maintain clonal diversity in their aphid hosts.     

The response of aphid secondary parasitoids to different patch densities of their host

Aphids are attacked by a large guild of natural enemies including many primary parasitoids which mummify their hosts. These mummies are themselves attacked by a guild of mummy parasitoids which are potentially important in regulating primary parasitoids at densities below which they can exert biological control. The response of mummy parasitoids to mummy densities was investigated in an experiment in which mummy densities of the pea aphid (Acyrthosiphon pisum) attacked by the parasitoid Aphidius ervi were manipulated across host plant patches. Overall, the risk of parasitism was density independent, though with very high inter-patch variability which may allow probabilistic refuges from secondary parasitism. Six species of four genera of mummy parasitoids were recorded. Of the responses of the individual genera, Coruna were reared most frequently from patches of high host density while amongst patches from which Syrphophagus was reared parasitism was inversely density dependent.     

Intraguild interactions in aphid parasitoids

We reviewed the literature on aphid parasitoids to determine the occurrence, nature and outcome of intraguild interactions. Intraguild interactions were described for larval, pupal and adult aphid parasitoids and by the type of natural enemy (fungus, predator, or parasitoid). They appear to be prevalent in most aphid parasitoid systems and, except for parasitoid-parasitoid interactions, they are mostly asymmetric, with aphidophagous predators and pathogens killing parasitoids. The limited experimental evidence from field studies is insufficient to provide a comprehensive pattern of the consequences of intraguild interactions for aphid parasitoid populations in general and, more specifically, for the efficacy of biological control. However, because intraguild interactions are widespread in aphid-natural enemy communities and mostly detrimental to aphid parasitoids, we conclude that intraguild interactions have a primary effect in driving fluctuations in aphid parasitoid populations. Drawing on case studies, we further argue that intraguild interactions can substantially alter the effectiveness of aphid parasitoids as biological-control agents.     

Endoparasitism in cereal aphids: molecular analysis of a whole parasitoid community

Insect parasitoids play a major role in terrestrial food webs as they are highly diverse, exploit a wide range of niches and are capable of affecting host population dynamics. Formidable difficulties are encountered when attempting to quantify host–parasitoid and parasitoid–parasitoid trophic links in diverse parasitoid communities. Here we present a DNA-based approach to effectively track trophic interactions within an aphid–parasitoid food web, targeting, for the first time, the whole community of parasitoids and hyperparasitods associated with a single host. Using highly specific and sensitive multiplex and singleplex polymerase chain reaction, endoparasitism in the grain aphid Sitobion avenae (F) by 11 parasitoid species was quantified. Out of 1061 aphids collected during 12 weeks in a wheat field, 18.9% were found to be parasitized. Parasitoids responded to the supply of aphids, with the proportion of aphids parasitized increasing monotonically with date, until the aphid population crashed. In addition to eight species of primary parasitoids, DNA from two hyperparasitoid species was detected within 4.1% of the screened aphids, with significant hyperparasitoid pressure on some parasitoid species. In 68.2% of the hyperparasitized aphids, identification of the primary parasitoid host was also possible, allowing us to track species-specific parasitoid-hyperparasitoid links. Nine combinations of primary parasitoids within a single host were found, but only 1.6% of all screened aphids were multiparasitized. The potential of this approach to parasitoid food web research is discussed.     

Structure of a herbivore–parasitoid community: Are parasitoids shared by different herbivore guilds?

Plant–herbivore–parasitoid interactions are a common occurrence in terrestrial food webs. Few parasitoids are thought to be shared by host insects of different feeding guilds because different parasitism strategies are required to use hosts of different feeding types. However, this assumption has rarely been tested using data from nature. To clarify whether parasitoids are shared among host guilds, I examined the structure of parasitoid communities on herbivore guilds associated with two Rhododendron species (Ericaceae) in a temperate secondary forest in central Japan. Leaf- and flower-feeding insects were collected from Rhododendron reticulatum and Rhododendron macrosepalum shrubs and reared in the laboratory for 3 years from April 1999 to March 2002. In total, 79 species of holometabolous herbivores (Lepidoptera, Diptera, Coleoptera, and Hymenoptera) were recorded, with 62 species on R. reticulatum and 51 species on R. macrosepalum. A total of 81 parasitoid species (Hymenoptera and Diptera) was recorded from the sampled herbivores, with 48 species from those on R. reticulatum and 50 species from those on R. macrosepalum. In total, 36 herbivore species were parasitised by 1–18 parasitoid species per host species, although the number of parasitoid species was strongly affected by sample size. Parasitoids that had two or more host species frequently attacked herbivore species from different families or on different host plants, whereas they did not attack species from different herbivore guilds; no parasitoids were shared between external feeders and rollers. Therefore, my results support the hypothesis that few parasitoids are shared among herbivores of different feeding guilds.     

The influence of aphid-produced honeydew on parasitoid fitness and nutritional state: A comparative study

Honeydew is a sugar-rich resource excreted by many hemipteran species and is a key food source for other insect species such as ants and parasitoid wasps. Here, we evaluated the nutritional value of 14 honeydews excreted by 13 aphid species for the generalist aphid parasitoid Lysiphlebus testaceipes to test a series of hypotheses concerning variation in the nutritional value of honeydew. There was a positive correlation between the body sugar content of honeydew-fed parasitoids and their longevity. This information is valuable for biological control researchers because it demonstrates that the nutritional state of honeydew-fed parasitoids in the wild can indicate their fitness, independently of the honeydew source they have fed on.Although the carbohydrate content and longevity of L. testaceipes differed greatly among the different honeydews, we did not find a significant effect of aphid or host plant phylogeny on these traits. This result suggests that honeydew is evolutionarily labile and may be particularly subject to ecological selection pressures. This becomes apparent when considering host aphid suitability: Schizaphis graminum, one of the most suitable and commonly used hosts of L. testaceipes, produced honeydew of the poorest quality for the parasitoid whereas Uroleucon sonchi, one of the few aphids tested that cannot be parasitized by L. testaceipes, excreted the honeydew with the highest nutritional value. These data are consistent with the hypothesis that hemipterans are subject to selection pressure to minimize honeydew quality for the parasitoids that attack them.     

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.     

The nutritional value of aphid honeydew for non-aphid parasitoids

Intake of sugar-rich foods by adult parasitoids is crucial for their reproductive success. Hence, the availability of suitable foods should enhance the efficacy of parasitoids as biological control agents. In situations where nectar is not readily available, homopteran honeydew can be a key alternative food source. We studied the impact of honeydew feeding on the longevity of the larval endoparasitoids Cotesia marginiventris, Campoletis sonorensis and Microplitis rufiventris, all natural enemies of important lepidopteran pests. Females of these wasps lived longer when feeding on honeydew produced by the aphid Rhopalosiphum maidis on barley compared to control females provided with water only. However, they lived shorter than females fed with a sucrose solution. Further investigations with C. marginiventris showed that access to honeydew also increases the number of offspring produced, but less so than access to a sucrose solution. Moreover, it was found that females of this species need to feed several times throughout their life in order to reach optimal longevity and reproductive output. Analyses of the sugars in the honeydew produced by R. maidis on barley revealed that it contains mainly plant-derived sugars, but also several aphid-synthesized sugars. The sugar composition of the honeydew changed as a function of aphid colony size and time a colony had been feeding on a plant. In general, the higher the aphid infestation, the smaller the percentage of aphid-synthesized sugars in the honeydew. Experiments with honeydew sugar mimics allowed us to reject the hypothesis that the relatively poor performance of the parasitoid on a honeydew diet was due to the sugar composition. Instead, the results from additional feeding experiments with diluted honeydew showed that the nutritional value of pure honeydew is primarily restricted by its high viscosity. The possible consequences of these findings for biological pest control are discussed.     

Adult parasitoids of the southern pine beetle, Dendroctonus frontalis Zimmermann (Coleoptera: Scolytidae), feed on artificial diet on pine boles, pine canopy foliage and understory hardwood foliage

This study examined adult parasitoids of Dendroctonus frontalis Zimmermann (Coleoptera: Scolytidae) utilizing an artificial parasitoid food on locations with and without hosts. Eliminade™ was applied to bark on boles of infested pines, to pine canopy foliage and to understory hardwood foliage. Adult parasitoids were collected, identified and dissected to determine the presence of Eliminade™ within their guts. Individuals from eight parasitoid species were collected on pine boles within D. frontalis infestations in the Talladega National Forest (Alabama) in the summer of 1999 and 2000. Mean percentage of parasitoids feeding on Eliminade™ was 62±10% during both summers. Percentage of parasitoids feeding was the same 24 h after Eliminade™ application, regardless of food location or parasitoid species. Seven days later, level of parasitoid feeding on Eliminade™ was insignificant in the pine canopy and hardwood understory. In contrast, percent of parasitoid feeding on Eliminade™ applied to pine boles remained the same between 1 and 7 days of the application. Therefore, not only will adult parasitoids visit and feed on artificial food on pine boles with hosts, but also non-host locations such as pine canopy and understory hardwood foliage. These results have implications for potential sources of adult nutrition for parasitoids of D. frontalis.     

中国菌食性管蓟马物种多样性及分布格局

菌食性管蓟马是土壤动物的重要组分, 它们在生物多样性保护与利用、植物保护、动物地理等领域具有重要的研究价值, 但在我国其分类和物种多样性研究仍有较大不足, 大尺度分布格局形成原因也不清楚。本文基于对我国大部分地区广泛的野外采集调查和国内外多家研究机构馆藏标本的检视, 整理了我国菌食性管蓟马物种名录和地理分布信息, 总结了我国菌食性管蓟马的分类研究现状与简史, 分析了菌食性管蓟马物种多样性的分布格局并探讨了该格局形成原因。目前我国记录菌食性管蓟马237种, 其中管蓟马亚科39属156种, 灵管蓟马亚科22属81种; 竹管蓟马属(Bamboosiella)、剪管蓟马属(Psalidothrips)、网管蓟马属(Apelaunothrips)和全管蓟马属(Holothrips)是物种较多的属, 包含物种数均超过10种; 中国特有73种; 广东、台湾、海南和云南是物种最丰富的省份, 均超过60种, 这些省份都具热带和亚热带气候特征, 适合其生存; 相对多度分析结果表明在热带和亚热带地区森林凋落物层菌食性管蓟马是土壤动物的常见类群; 气温、降水量、食物等是限制其分布的主要因素。本结果丰富了土壤生物多样性的研究内容, 为菌食性管蓟马多样性大尺度空间格局研究提供了数据支持。     

Plant Species Loss Affects Life-History Traits of Aphids and Their Parasitoids

The consequences of plant species loss are rarely assessed in a multi-trophic context and especially effects on life-history traits of organisms at higher trophic levels have remained largely unstudied. We used a grassland biodiversity experiment and measured the effects of two components of plant diversity, plant species richness and the presence of nitrogen-fixing legumes, on several life-history traits of naturally colonizing aphids and their primary and secondary parasitoids in the field. We found that, irrespective of aphid species identity, the proportion of winged aphid morphs decreased with increasing plant species richness, which was correlated with decreasing host plant biomass. Similarly, emergence proportions of parasitoids decreased with increasing plant species richness. Both, emergence proportions and proportions of female parasitoids were lower in plots with legumes, where host plants had increased nitrogen concentrations. This effect of legume presence could indicate that aphids were better defended against parasitoids in high-nitrogen environments. Body mass of emerged individuals of the two most abundant primary parasitoid species was, however, higher in plots with legumes, suggesting that once parasitoids could overcome aphid defenses, they could profit from larger or more nutritious hosts. Our study demonstrates that cascading effects of plant species loss on higher trophic levels such as aphids, parasitoids and secondary parasitoids begin with changed life-history traits of these insects. Thus, life-history traits of organisms at higher trophic levels may be useful indicators of bottom-up effects of plant diversity on the biodiversity of consumers.     

The scaling of body size and mass in a host-parasitoid association: influence of host species and stage

We describe the allometry of body mass and body size as measured by hind-tibia length in males of Monoctonus paulensis (Ashmead) (Hymenoptera: Braconidae, Aphidiinae), a solitary parasitoid of aphids. To assess the influence of host quality on allometric relationships, we reared parasitoids on second and fourth nymphal instars of four different aphid species, Acyrthosiphon pisum (Harris), Macrosiphum creelii Davis, Myzus persicae (Sulzer) and Sitobion avenae (F.), under controlled conditions in the laboratory. Dry mass was positively correlated with hind-tibia length, and could be predicted from it, in unparasitized aphids, in aphid mummies containing parasitoid pupae, and in the parasitoid. The reduced-major-axis scaling exponents for the regression of dry mass on hind-tibia length were species-specific in aphids, reflecting differences in volume and shape between species. In mummified aphids, the stage at death influenced the size/mass relationship. In males of M. paulensis, the allometric exponent varied between parasitoids developing in different kinds of host. Individuals developing in pea aphid were absolutely larger in dry mass as well as proportionately larger relative to their hind-tibia length. We discuss the allometry of body size and body mass in relation to parasitoid fitness.     

Generalist predators disrupt parasitoid aphid control by direct and coincidental intraguild predation

Generalist predators and parasitoids are considered to be important regulators of aphids. The former not only feed on these pests, but might also consume parasitoids at all stages of development. This direct or coincidental interference affects the natural control of aphids, the scale of which is largely unknown, and it has rarely been examined under natural conditions. Here, molecular diagnostics were used to track trophic interactions in an aphid-parasitoid-generalist predator community during the build-up of a cereal aphid population. We found that generalist predators, principally carabid and staphylinid beetles as well as linyphiid spiders, had strong trophic links to both parasitoids and aphids. Remarkably, more than 50% of the parasitoid DNA detected in predators stems from direct predation on adult parasitoids. The data also suggest that coincidental intraguild predation is common too. Generalist predators, hence, disrupt parasitoid aphid control, although the levels at which the predators feed on pests and parasitoids seem to vary significantly between predator taxa. Our results suggest that taxon-specific trophic interactions between natural enemies need to be considered to obtain a more complete understanding of the route to effective conservation biological control.     

Bidirectional movement of aphid parasitoids (Braconidae: Aphidiinae) between crops and non-crop plants in agroecosystems of central Argentina

The movement of predators and parasitoids between natural and cultivated habitats is a common process in agroecosystems, which may be affected by different biotic and abiotic factors, mostly related to the availability of resources. Here, through a broad approach, we aimed to obtain an overview of factors affecting the bidirectional movement of aphid parasitoids (Braconidae: Aphidiinae) across cultivated habitats and their natural vegetated borders. Using bidirectional flight traps, we measured the number of parasitoids moving from borders to crops and vice versa, in fields of three common crop species (alfalfa, oat and wheat) in the Pampean region, Santa Fe, Argentina. The effects of the abundance of aphid prey, abundance and richness of flowers in both habitats, as well as temperature and wind speed on parasitoid movement, were assessed through generalized mixed models, considering sampling date and field as random factors. The relationship between parasitism percentages and parasitoid movement from the borders to the crops was explored separately for three pest aphid species: Aphis craccivora Koch, Rhopalosiphum padi (L.) and Schizaphis graminum (Rondani). Overall, we found a prevalence of parasitoids moving in the border-crop direction, mainly in wheat and alfalfa crops. Aphid abundance in the arrival habitat affected parasitoid movement in both directions. A link between parasitoid movement and parasitism percentages was observed for the aphid species S. graminum in wheat, suggesting a beneficial role of natural vegetation in pest control.     

Impact of a parasitoid on the bacterial symbiosis of its aphid host

Embryo production in aphids is absolutely dependent on the function of symbiotic bacteria, mainly Buchnera, and the growth and development of koinobiont parasitoids in aphids requires the diversion of nutrients from aphid embryo production to the parasitoid. The implication that the bacterial symbiosis may be promoted in parasitized aphids to support the growing parasitoid was explored by analysis of the number and biomass of mycetocytes, and the aphid cells bearing Buchnera, in the pea aphid Acyrthosiphon pisum Harris (Hemiptera: Aphididae) parasitized by the wasp Aphidius ervi Haliday (Hymenoptera: Braconidae). Aphids hosting a young larval parasitoid bore more mycetocytes of greater total biomass, and embryos of lower biomass than unparasitized aphids. Furthermore, one of the three aphid clones tested, which limited teratocyte growth (giant cells of parasitoid origin having a trophic role), bore smaller mycetocytes and larger embryos, than one or both of the two aphid clones with greater susceptibility to the parasitoid. These data suggest that susceptibility of the aphid‐Buchnera symbiosis to parasitoid‐mediated manipulation may, directly or indirectly, contribute to aphid susceptibility to parasitoid exploitation.     

Combining lacewings and parasitoids for biological control of foxglove aphids in sweet pepper

The role of natural enemy diversity in biological pest control has been debated in many studies, and understanding how interactions amongst predators and parasitoids affect herbivore populations is crucial for pest management. In this study, we assessed the individual and combined use of two species of natural enemies, the parasitoid Aphidius ervi Haliday, and the predatory brown lacewing Micromus variegatus (Fabricius), on their shared prey, the foxglove aphid, Aulacorthum solani (Kaltenbach), on sweet pepper. We hypothesized that the presence of intraguild predation (IGP) and predator facilitation (through induced aphid dropping behaviour) might have both negative and positive effects on aphid control, respectively. Our greenhouse trial showed that overall, the greatest suppression of aphids occurred in the treatment with both the parasitoid and the lacewing. While the combination of lacewings and parasitoids significantly increased aphid control compared to the use of parasitoids alone, the effect was not significantly different to the treatment with only predators, although there was a clear trend of enhanced suppression. Thus, the combined effects of both species of natural enemies were between additive and non‐additive, suggesting that the combination is neither positive nor negative for aphid control. High levels of IGP, as proven in the laboratory, were probably compensated for by the strong aphid suppression provided by the lacewings, whether or not supplemented with some level of predator facilitation. For aphid management over a longer time scale, it might still be useful to combine lacewings and parasitoids to ensure stable and resilient aphid control.