Aphid Mummies Research Articles

A molecular approach to unravel trophic interactions between parasitoids and hyperparasitoids associated with pecan aphids.

Advances in molecular ecology can overcome many challenges in understanding host-parasitoid interactions. Genetic characterization of the key-players in systems helps to confirm species and identify trophic linkages essential for ecological service delivery by biological control agents; however, relatively few agroecosystems have been explored using this approach. Pecan production consists of a large tree perennial system containing an assortment of seasonal pests and natural enemies. As a first step to characterizing host-parasitoid associations in pecan food webs, we focus on aphid species and their parasitoids. Based on DNA barcoding of field-collected and reared specimens, we confirmed the presence of 3 species of aphid, one family of primary parasitoids, and 5 species of hyperparasitoids. By applying metabarcoding to field-collected aphid mummies, we were able to identify multiple species within each aphid mummy to unravel a complex food web of 3 aphids, 2 primary parasitoids, and upward of 8 hyperparasitoid species. The results of this study demonstrate that multiple hyperparasitoid species attack a single primary parasitoid of pecan aphids, which may have negative consequences for successful aphid biological control. Although further research is needed on a broader spatial scale, our results suggest multiple species exist in this system and may suggest a complex set of interactions between parasitoids, hyperparasitoids, and the 3 aphid species. This was the first time that many of these species have been characterized and demonstrates the application of novel approaches to analyze the aphid-parasitoid food webs in pecans and other tree crop systems.

Flowering areas enhance insect pollinators and biological control agents in wheat intensive agro‐ecosystems

Abstract This 4‐year study (2018–2021) aimed at investigating the effects of flowering areas inserted at the margin of soft wheat fields (Triticum aestivum L.) in comparison with spontaneous field margins. The action formed part of a multidisciplinary initiative promoted by the Barilla food company, aimed at promoting the sustainable production of soft wheat. Specific aims were to study the effects of flowering areas on (i) the abundance and species richness of insect pollinators, including wild bees, syrphids and butterflies; (ii) the levels of wheat aphid and bug infestations and (iii) the assemblages of biological control agents of aphids (coccinellids and aphid mummies as a result of parasitization). Insect surveys were carried out on 61 wheat‐growing farms located in Northern Italy. Insect pollinators were sampled on all farms, whereas wheat aphids, wheat bugs and aphid biological control agents were investigated in a sub‐sample of 20 farms. Results generally indicated a positive impact of flowering areas on multiple taxa in comparison with spontaneous field margins. The abundance of pollinators and coccinellids was significantly enhanced by the flowering areas. Aphid mummies showed an interaction between strategies and distances with more mummies at 5 m in wheat plots close to flowering areas and at 50 m in the plots close to spontaneous field margin (control). Flowering areas were validated as an important tool for promoting beneficial taxa in agro‐ecosystems. However, the successful establishment of this ecological infrastructure was suggested to rely on several factors, which included both the selection of suitable flowering plant species and the implementation of appropriate management practices.

Short- and long-term effects of commercial formulations of imidacloprid, spirotetramat, and mixtures of these active ingredients on pupae of Diaeretiella rapae (Hymenoptera: Braconidae) and its progeny.

Compatibility studies of insecticides and natural enemies usually focus on short-term lethal effects, without considering the long-term sublethal effects (including progeny). Even less-explored are the effects of commercial insecticides formulated with more than one active product. Short- and long-term lethal and sublethal effects were studied for the first time on the progeny of commercial formulations of spirotetramat, imidacloprid and a commercial mixture of these active ingredients on pupae of Diaeretiella rapae (M'ntosh) (Hymenoptera: Braconidae), an endoparasitoid of aphids considered to be a potential biological control agent. Insecticides were exposed topically on aphid mummies in which the parasitoid was in the pupal stage. Imidacloprid reduced adult emergence by more than 30% and prolonged intra-host development time with respect to control from half the maximum recommended field dose (MFRD). Spirotetramat and commercial mixture only showed significant effects on these endpoints at doses above the MFRD. The tested formulations did not affect adult longevity, sex ratio, and percentage of parasitism in the exposed generation. At low concentrations the active ingredients in the commercial mixture behave synergistically, whereas at medium and high concentrations they behave antagonistically. Considering the 10% lethal dose (LD10), imidacloprid showed the highest hazard coefficient, whereas the commercial mixture was more hazardous when considering the LD50 and LD90. The commercial mixture and imidacloprid induced higher adult emergence and altered the sex ratio in the progeny. The following order of toxicity on D. rapae can be established: imidacloprid > commercial mixture > spirotetramat. Joint use of this species with imidacloprid and commercial mixture should be avoided in integrated pest management programs. © 2024 Society of Chemical Industry.

The effects of insecticide seed treatments on the parasitism and predation of Myzus persicae (Homoptera: Aphididae) in canola.

The green peach aphid, Myzus persicae (Sulzer) (Homoptera: Aphididae), is a major pest of brassica plants, with the ability to transmit > 100 viruses. Although the adoption of Integrated Pest Management is increasing, chemical treatment remains the predominant method used to control M. persicae globally. Insecticide seed treatments, typically with neonicotinoid active ingredients, have become commonplace in canola crops, and are viewed as a "softer" alternative to foliar sprays but may nevertheless impact natural enemies of M. persicae. In this study, the effects of canola seed treatments, containing imidacloprid, thiamethoxam, and a mixture of thiamethoxam + lambda-cyhalothrin, were investigated on the parasitoid wasp, Aphidius colemani Viereck (Hymenoptera: Braconidae) and the green lacewing, Mallada signatus (Schneider) (Neuroptera: Chrysopidae), both important natural enemies of M. persicae. Laboratory trials were undertaken using whole plants, with lethal and sublethal effects assessed by measuring several traits. Compared with untreated plants, more aphid mummies were produced and more A. colemani were reared on plants treated with thiamethoxam + lambda-cyhalothrin and more aphid mummies were produced on imidacloprid plants. Imidacloprid reduced the time A. colemani spent searching for M. persicae and thiamethoxam reduced its cleaning time. However, after A. colemani were removed from treated plants, there were no such effects observed, suggesting these impacts were relatively short-lived. We found no significant effects of seed treatments on M. signatus. These results point to the complexity of ecotoxicology studies involving multiple trophic levels and indicate that seed treatments may have variable impacts on key fitness traits of natural enemies.

Canopy hedge pruning in pecan production differentially affects groups of arthropod pests and associated natural enemies

Controlling canopy growth and size through pruning techniques in perennial agroecosystems is often crucial to maximizing productivity. However, the implications of modifying canopy architecture for arthropod management are often overlooked. We studied the effects of hedge pruning on pests and natural enemies on mature pecan trees by assessing the abundance of: 1) leaf-dwelling aphids and mites, 2) visually detectable injuries caused by black pecan aphids [Melanocallis caryaefoliae (Davis)] and Phylloxera spp., 3) aphid parasitoids and parasitized hosts (aphid mummies), and 4) predatory mites. Additionally, we assessed the prevalence of entomopathogens that dwell on the orchard floor, under the trees. Hedge pruning decreased Phylloxera infestation but increased pressure from scorch mites and the yellow aphid complex. Black pecan aphid abundance responded inconsistently, but their damage was consistently reduced in hedged canopies. Predatory mites were only affected by hedging in the second year when higher populations were observed. Although parasitoid wasp abundance was not affected by hedging, more parasitized aphids (mummies) were observed in trees that did not receive pruning in the first year. Also, higher activity of entomopathogens was observed in soil cores collected under hedged trees in the first year but lower in the second. Taken together, the effects of hedge pruning pecan canopies were case-specific, and cannot be generalized across pests or natural enemies. Nevertheless, structural and environmental variation across seasons and within hedge pruning systems clearly have implications for crop protection in pecans and other perennial systems.

Host Range and Phenology of Sugarcane Aphid (Hemiptera: Aphididae) and Natural Enemy Community in Sorghum in Haiti.

To determine the factors leading to outbreaks of the sugarcane aphid, Melanaphis sacchari, (Zehntner) (Hemiptera: Aphididae) in sorghum in Haiti, a survey was carried out on farms during two cropping seasons, spring and fall of 2018. A total of 45 plots in three Haitian regions were monitored from the five-leaf stage to grain ripening. Infestation with M. sacchari was significantly higher in spring than in fall, except in one location. Melanaphis sacchari populations varied significantly according to phenological stages of sorghum, with significantly higher abundance during the heading and flowering stages than other stages. In and around sorghum fields, the sugarcane aphid was observed on plants from three families: Poaceae, Malvaceae, and Cucurbitaceae. Aphid natural enemies found in sorghum fields consisted of eight species of ladybeetles (Coleoptera: Coccinellidae), one hoverfly (Diptera: Syrphidae), one lacewing (Neuroptera: Chrysopidae), and one predatory midge (Diptera: Cecidomyiidae). In addition to these predators, two parasitoid species, Adialytus sp. (Hymenoptera: Braconidae) and Pachyneuron aphidis (Bouché) (Hymenoptera: Pteromalidae), emerged from sugarcane aphid mummies. Predator and parasitoid densities were highly affected by growing season, with most of the biological control happening in fall. This study provides insights on sugarcane aphid management in Haiti and the Caribbean Islands.

Evaluation of the Effect of Fungatol and Gamma-T-ol on the Emergence and Adult Parasitoid Survival of Mummies of Cotton Aphids Parasitized by Aphidius colemani.

Simple SummaryBiological control can be used as an alternative control measure to reduce pesticide resistance. Unfortunately, many biological control agents, such as natural enemies of pests, are susceptible to a broad spectrum of pesticides. This creates a potential problem when these two components are utilized together. Therefore, it is necessary to find alternatives that are not harmful to natural enemies but also have the potential to replace synthetic pesticides. Essential oils (EOs) are widely used in crop protection and organic agriculture. The EO formulations evaluated in this study are new botanical pesticides that play an important role in agriculture. EOs are available as an alternative to synthetic pesticides. Two blends (Fungatol and Gamma-T-ol) are mostly composed of Alpha Tops, and Gamma Tops were assessed for their effects on the aphid parasitoid Aphidius colemani in laboratory and glasshouse trials. According to the International Organization for Biological Control (IOBC) classification, they were found to be safe or only slightly toxic, making them potential candidates for introduction into an integrated pest control program for aphids.Beneficial insects play a major role in controlling pest populations. In sustainable agricultural production systems, control methods compatible with integrated pest management (IPM) are preferred over broad-spectrum pesticides. EOs from aromatic plants may provide a new and safe alternative to synthetic chemicals. In this research, the efficacy of Fungatol, Gamma-T-ol, Fungatol plus neem, and Gamma-T-ol plus neem was evaluated against Aphidius colemani Viereck (Hymenoptera: Braconidae; Aphidiidae), the parasitoid of the cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae). Under laboratory and greenhouse conditions, five different concentrations of each formulation were applied to parasitized mummies and adult parasitoids. Results for parasitoid emergence from aphid mummies sprayed with different concentrations of Fungatol, Gamma-T-ol, Fungatol plus neem, and Gamma-T-ol plus neem in the laboratory and glasshouse showed that the formulations did not adversely affect adult emergence as rates above 60% were observed. For residual toxicity tests done by exposing adult parasitoids to a fresh, dry biopesticide film sprayed on glass plates, less than 20% mortality was observed after 48 h of exposure. Adult longevity tests revealed that the highest concentrations of some of the formulations evaluated were slightly toxic to A. colemani. According to the IOBC rating, our results indicated that most of the tested concentrations for each formulation were harmless to A. colemani. Based on the above results, it may be proposed that the formulations evaluated in this study are potential botanical pesticide candidates for incorporation into an IPM program.

Effects of Prohydrojasmon on the Number of Infesting Herbivores and Biomass of Field-Grown Japanese Radish Plants.

Prohydrojasmon (PDJ), an analog of jasmonic acid (JA), was found to induce direct and indirect defenses against herbivores in non-infested plants. To test whether PDJ can be used for pest control in crop production, we conducted experiments in pesticide-free Japanese radish fields from October 4 to December 12 in 2015. Twenty-four Japanese radish plants in three plots were treated with a 100 times-diluted commercial formulation (5%) of PDJ (treated plants), and 24 plants in three different plots were treated with water (control plants) until November 29 every week. Throughout the observation period, the number of aphids, leaf-mining fly larvae, vegetable weevils, and thrips was significantly lower on the treated plants than on the control plants. In contrast, the number of lepidopteran larvae was not significantly different between the treated and control plants throughout the study period. Parasitized aphids (mummies) were also observed in both plots. Poisson regression analyses showed that a significantly higher number of mummies was recorded on the treated plants as compared to that on the control plants when the number of aphids increased. This suggested that PDJ application to Japanese radish plants attracted more parasitoid wasps on the treated plants than on the control plants. We also identified eight terpenoids and methyl salicylate as the PDJ-induced plant volatiles in the headspace of the treated plants. Some of these volatiles might be responsible for attracting aphid-parasitoid wasps in the field. However, for other insect pests, we did not find any natural enemies. Interestingly, the genes of the JA and salicylic acid signaling pathways were differentially upregulated in the treated plants. We also observed that the PDJ treatments induced the expression of the genes related to glucosinolate biosynthesis and the subsequent isothiocyanate formation. Additionally, the weights of both the aboveground and belowground parts of the treated plants were significantly lower than those of the respective parts of the control plants. These results indicated that the treatment of Japanese radish plants with a 100 times-diluted commercial formulation of PDJ induced their direct and indirect defenses against several insect pest species to reduce their numbers, and negatively affected their biomass.

Multisite Seasonal Monitoring of Pecan Aphids and Their Parasitoid in Commercial Pecan Orchards.

Aphids are important pests of pecans in Georgia. Although previous studies conducted seasonal monitoring of pecan aphids, these studies were done at a single experimental site. In addition, only a few seasonal monitoring studies have tracked pecan aphid mummies parasitized by the aphid parasitoid, Aphelinus perpallidus Gahan. The objective of this study was to assess the seasonal phenology of yellow pecan aphid (Monelliopsis pecanis Bissell), blackmargined aphid [Monellia caryella (Fitch)], black pecan aphid [Melanocallis caryaefoliae (Davis)], aphid mummies, and adult A. perpallidus in four Georgia commercial orchards, with varying aphid management regimes, in 2019 and 2020. Comparison of overall aphid and parasitoid numbers between sites revealed few consistent annual patterns in both years. Aphid seasonal trends were consistent among sites and followed the patterns seen in previous studies, with the yellow aphid complex peaking in May, June, September, and October and black pecan aphids peaking in late September and October. Despite varying levels of insecticide application between sites, aphid phenology followed a similar seasonal pattern and remained low, throughout both growing seasons. This may indicate that growers can apply low frequencies of insecticides and still achieve pecan aphid control. Parasitism numbers were highest in the low insecticide frequency site compared with the other three sites. Mummies varied in their correlation with yellow aphid complex and black pecan aphid numbers. Parasitoid numbers typically followed the cycle of their host throughout the season.

Neighbourhood effect of faba bean (Vicia faba L.) on density of vegetation-dwelling natural biocontrol agents in winter wheat

Legume crops such as faba bean (Vicia faba L.) have been underrepresented in conventional cropping systems in Europe for decades for economic reasons, even though faba bean is a native crop and suitable to diversify local cropping systems. While the environmental benefits that go along with faba bean cropping are well established, there is a gap of knowledge on the effects faba bean may have on biodiversity and associated ecosystem services, such as natural biocontrol in agricultural landscapes.The aim of the present field study was to quantify neighbourhood effects of faba bean on densities of vegetation- dwelling natural biocontrol agents and herbivores in adjacent winter wheat. Densities of predators, herbivores, parasitized aphids (mummies) and leaf damage by the cereal leaf beetle (CLB) were assessed by repeated visual counts in conventionally managed winter wheat crops. In winter wheat adjacent to faba bean, total predator density was higher than in wheat adjacent to winter wheat, independent of the observation period. This effect was not reflected in the predator-prey ratio though. The total density of mummies and parasitism rate were not affected by the neighbouring faba bean crop. Predator density decreased towards the field centre. CLB leaf damage and yield were not affected by the neighbouring crop. All densities were affected by the observation period. The effects were measurable in spite of the external management such as insecticide application, which had a negative effect on both predator and herbivore densities. The present study sheds first light on faba bean effects on natural biocontrol agents in conventionally managed agro-ecosystems. While few, effects were measurable, which shows the need for further research on the association of faba bean cropping with the ecosystem service natural biocontrol.

Botanical formulations for the ecological management of Myzus persicae (Sulzer) and Aphis gossypii (Clover) (Hemiptera: Aphididae) and their side effects on parasitoids

The peach aphid Myzus persicae (Sulzer) and cotton aphid Aphis gossypii (Clover) (Hemiptera: Aphididae) are considered to be key pests affecting greenhouse pepper crops in Argentina as a result of their frequent occurrence and the seriousness of the damage caused by their feeding behavior and the transmission of virus. The goal of this research was to determine the efficiency of botanical products to control aphids and their side effects on parasitoids in this crop. Thus, three biorational pest control formulations derived from essential oils (EO) and plant extracts (Es) were tested, namely (i) neem EO, cinnamon EO, clove EO, oregano EO and American marigold EO (formulation 1); (ii) garlic EO and cinnamon EO (formulation 2); (iii) garlic E and rue E (formulation 3); and a soy lecithin adjuvant (lecithin), and finally, a control (water spray method). For this research, a completely randomized design was replicated 3 times. These treatments were applied directly to the foliage by means of a backpack sprayer on a weekly basis until the end of this trial. Subsequently, the total number of healthy aphids and parasitized aphids (mummies) on every leaf was recorded in the field and the laboratory through repeated measures Analysis of Variance (ANOVA) and LSD Fisher method. The results showed that formulation 1 and formulation 3 recorded a lower number of aphids and mummies compared to the other treatments. This evidence would demonstrate that these formulations repel aphids and parasitoids without the lethal effects caused by the use of broad spectrum insecticides.

Plant silicon application alters leaf alkaloid concentrations and impacts parasitoids more adversely than their aphid hosts.

Grasses accumulate large amounts of silicon (Si) which acts as a highly effective physical defence against insect herbivory, however recent evidence shows that Si supplementation also modifies plant secondary metabolite concetrations. Changes in plant secondary metabolites concentrations can have cascading effects on higher trophic levels, such as parasitoids, as they are dependent on the host herbivore for growth and development. However, relatively little is known about how Si application affects higher trophic levels. We examined the effects of Si addition on alkaloid content in leaves of Phalaris aquatica (Poaceae) and the effect on interactions between an aphid (Rhopalosiphum padi) and its parasitoid (Aphidius colemani). Si supplementation had no effect on aphid abundance or parasitism rate. Adult aphids, aphid mummies (parasitised aphids) and the emergent parasitoids were, however, significantly smaller on Si+ plants. Parasitoid traits (size and emergence) were correlated with aphid mummy size. Si addition reduced parasitoid emergence rate and size due to reduced host mummy size, in addition, significantly fewer females emerged from mummies on Si+ plants. Aphid infestation significantly altered alkaloids concentrations, reducing gramine by 80% while increasing tryptamine by 91% in Si- plants. Si addition reduced aphid-induced tryptamine concentrations by 64% and increased 5-MeO-tryptamine by over 800% in control and 142% in aphid infested plants. Our results show that while Si addition has modest impacts on the herbivore, it significantly alters secondary metabolites and has stronger effects on the higher trophic level through changes in the quality of the parasitised host.

Semiochemicals and habitat manipulation to support green lacewing activity to reduce aphid infestations in agroecosystems

Conservation biological control (CBC) is a promising tool for ecological intensification that aims to establish resilient natural enemy populations that contribute to pest management with reduced use of pesticides and at the same time support native biodiversity in agroecosystems. Yet the impact of natural enemies in CBC is often limited due to missing resources such as food, habitat, and hibernation shelters. Here, we studied a CBC strategy that incorporates these essential resources combined with semiochemicals, focusing on how the common green lacewing can enhance biological control of aphids.In a 4-year field study conducted at three locations in the region of East Norway, we developed a CBC strategy combining the three measures ATTRACT (a ternary attractant that increase lacewing egg laying), FOOD (floral buffer strips), and SHELTER (insect hotels for overwintering survival) to increase aphid biological control in spring barley. We recorded the number of lacewings, ladybirds, hoverflies, parasitized aphid mummies, and the two cereal aphid species Sitobion avenae and Rhopalosiphum padi. Our CBC strategy resulted in a significant increase in lacewing activity and significant aphid suppression. At all three locations and over the 4-year period, aphid infestation was below the economic damage threshold in the field plots using CBC measures. In contrast, during two of the years, the density of the aphid infestation in the control plots was significantly above the damage threshold. We found evidence that use of the ternary attractant supported green lacewings but led to loss of ladybirds, hoverflies, and parasitoids, even though flower strips were used as alternative resources.Our study shows a promising increase in lacewing activity in the agricultural landscape and high biological control of aphids in barley. Long-term field studies are needed to evaluate the impact on non-target species and the agroecosystem before practical application of this approach can be considered.

Parasitization of the sugarcane aphid, Melanaphis sacchari, by commercially available aphid parasitoids

Identification of natural enemies of novel pests is important for the development of effective integrated pest management. Commercially available parasitoids used for control of arthropod pests have potential for enhancing biological control of invasive pests. The sugarcane aphid, Melanaphis sacchari (Hemiptera: Aphididae), is a new pest on sweet sorghum, Sorghum bicolor, in the USA. Surveys of M. sacchari have not detected any parasitoids in central Kentucky. In North America, Aphelinus abdominalis (Hymenoptera: Aphelinidae), Aphidius ervi (Hymenoptera: Braconidae), Aphidius colemani, and Aphidius matricariae are sold for aphid management. This study’s objective was to determine the host acceptance and suitability of M. sacchari for these parasitoid species. Host acceptance was assessed by counting attacks and oviposition strikes by parasitoids on M. sacchari. All parasitoid species accepted M. sacchari as a host in the parental generation (purchased adults) and the F1 generation (reared from M. sacchari). Host suitability was evaluated by transferring M. sacchari from host acceptance trials to caged sweet sorghum plants. Cages were monitored for aphid mummies and emerged adult parasitoids. Parental A. colemani produced the most mummies and adult parasitoids and reduced final M. sacchari numbers by 75%. A. ervi had a similar impact on M. sacchari populations but produced fewer mummies and adults. A. matricariae and A. abdominalis did not reduce M. sacchari populations. F1 parasitoids produced few adults and did not reduce M. sacchari populations. A. colemani demonstrated potential for field releases with the ability to use M. sacchari as a host and reduce aphid population growth.

Effect of parasitized prey on prey consumption, survival, growth, and development of Coccinella septempunctata L. (Coleoptera: Coccinellidae) under laboratory conditions

A study of interactions among natural enemies is important to develop a better biological control program. Among these interactions, one that is crucial is the consumption of parasitized prey by a predator. Feeding on aphid mummies could affect the predator as well as the parasitoid species. In this study, the effect of parasitized prey on prey consumption, survival, growth, and development of 4th instar larvae of the predatory species, Coccinella septempunctata L. (Coleoptera: Coccinellidae), as an active predator of aphids, was studied. Moreover, the effect of parasitized and mummified aphids on female fecundity was also evaluated. The green peach aphid, Myzus persicae Sulzer (Hemiptera: Aphididae) was used. Obtained results showed that the parasitized aphids, as a predatory food, significantly affected the predator. The prey consumption was highest on parasitized (24.10 ± 0.53) and lowest on mummified (9.75 ± 0.40) aphids. The survival rate was in the order of non-parasitized > parasitized > mummified. The mass gained by the 4th instar larvae of C. septempunctata was in the order of parasitized (26.25 mg ± 0.89) > non-parasitized (19.25 mg ± 0.86) > mummified aphids (10.20 mg ± 0.52), when fed on different prey. Developmental time of the predator was recorded highest, when it consumed mummified aphids (13.6 ± 0.39). As well, female fecundity was affected positively. The female was observed to lay the most eggs (323.55 ± 1.57) to have the highest number of hatched eggs (38.70 ± 0.92), and to have the highest egg mass (196.10 μg ± 1.22), when it consumed the parasitized aphids in contrast to non-parasitized and mummified aphids. It was also found that the type of prey did not affect the incubation period of the eggs.

Volatiles of bacteria associated with parasitoid habitats elicit distinct olfactory responses in an aphid parasitoid and its hyperparasitoid

Abstract To locate mating partners and essential resources such as food, oviposition sites and shelter, insects rely to a large extent on chemical cues. While most research has focused on cues derived from plants and insects, there is mounting evidence that indicates that micro‐organisms emit volatile compounds that may play an important role in insect behaviour. In this study, we assessed how volatile compounds emitted by phylogenetically diverse bacteria affected the olfactory response of the primary parasitoid Aphidius colemani and one of its secondary parasitoids, Dendrocerus aphidum. Olfactory responses were evaluated for volatile blends emitted by bacteria isolated from diverse sources from the parasitoid's habitat, including aphids, aphid mummies and honeydew, and from the parasitoids themselves. Results revealed that A. colemani showed a wide variation in response to bacterial volatiles, ranging from significant attraction over no response to significant repellence. Our results further showed that the olfactory response of A. colemani to bacterial volatile emissions was different from that of D. aphidum. Gas chromatography‐mass spectrometry analysis of the volatile blends revealed that bacterial strains repellent to A. colemani produced significantly higher amounts of esters, organic acids, aromatics and cycloalkanes than attractive strains. Strains repellent to D. aphidum produced significantly higher amounts of alcohols and ketones, whereas the strains attractive to D. aphidum produced higher amounts of the monoterpenes limonene, linalool and geraniol. Overall, our results indicate that bacterial volatiles can have an important impact on insect olfactory responses, and should therefore be considered as an additional, so far often overlooked factor in studying multitrophic interactions between plants and insects. A free Plain Language Summary can be found within the Supporting Information of this article.

Facultative bacterial endosymbionts shape parasitoid food webs in natural host populations: A correlative analysis

Facultative bacterial endosymbionts can protect their aphid hosts from natural enemies such as hymenopteran parasitoids. As such, they have the capability to modulate interactions between aphids, parasitoids and hyperparasitoids. However, the magnitude of these effects in natural aphid populations and their associated parasitoid communities is currently unknown. Moreover, environmental factors such as plant fertilization and landscape complexity are known to affect aphid–parasitoid interactions but it remains unclear how such environmental factors affect the interplay between aphids, parasitoids and endosymbionts.Here, we tested whether facultative endosymbionts confer protection to parasitoids in natural populations of the English grain aphid, Sitobion avenae, and if this is affected by plant fertilization and landscape complexity. Furthermore, we examined whether the effects of facultative endosymbionts can cascade up to the hyperparasitoid level and increase primary‐hyperparasitoid food web specialization.Living aphids and mummies were collected in fertilized and unfertilized plots within 13 wheat fields in Central Germany. We assessed the occurrence of primary parasitoid, hyperparasitoid and endosymbiont species in aphids and mummies using a newly established molecular approach.Facultative endosymbiont infection rates were high across fields (~80%), independent of whether aphids were parasitized or unparasitized. Aphid mummies exhibited a significantly lower share of facultative endosymbiont infection (~38%). These findings suggest that facultative endosymbionts do not affect parasitoid oviposition behaviour, but decrease parasitoid survival in the host. Facultative endosymbiont infection rates were lower in mummies collected from fertilized compared to unfertilized plants, indicating that plant fertilization boosts the facultative endosymbiont protective effect. Furthermore, we found strong evidence for species‐specific and negative cascading effects of facultative endosymbionts on primary and hyperparasitoids, respectively. Facultative endosymbionts impacted parasitoid assemblages and increased the specialization of primary‐hyperparasitoid food webs: these effects were independent from and much stronger than other environmental factors.The current findings strongly suggest that facultative endosymbionts act as a driving force in aphid–parasitoid–hyperparasitoid networks: they shape insect community composition at different trophic levels and modulate, directly and indirectly, the interactions between aphids, parasitoids and their environment.

Seasonal differences in the abundance of an ant-adapted parasitoid, Lysiphlebus japonicus (Hymenoptera: Aphidiidae), in ant-attended colonies of the spirea aphid Aphis spiraecola (Hemiptera: Aphididae) on citrus: comparison for two ant species, Lasius japonicus and Pristomyrmex punctatus (Hymenoptera: Formicidae)

The parasitoid Lysiphlebus japonicus Ashmead is able to exploit aphids attended by ants and is therefore a candidate for a biological control agent of ant-attended aphids, but there is little information on the factors that influence changes in the population of this parasitoid. The species of aphid-attending ants may be a factor in seasonal fluctuations in its occurrence. This study experimentally examined how each of the two ant species Lasius japonicus Santschi and Pristomyrmex punctatus Smith influences the seasonal change in the abundance of this ant-adapted parasitoid in the colonies of the spirea aphid Aphis spiraecola Patch, which the ant species attends, on citrus in Japan. The numbers of aphid mummies formed by the parasitoid and ovipositing parasitoid females in the ant-attended aphid colonies in late spring (mid- to late May) were compared with the numbers in mid-summer (late July to mid-August) for each ant species. Significantly more mummies were found in the aphid colonies attended by P. punctatus than in the colonies attended by Lasius japonicus in both seasons. The number of mummies in P. punctatus-attended aphid colonies did not differ significantly between the two seasons. In the Lasius japonicus-attended colonies, however, the mummy numbers were significantly reduced in mid-summer compared with late spring. The seasonal distribution of mummy numbers was significantly dependent on the aphid-attending ant species. The number of parasitoid females that deposited eggs in the ant-attended aphid colonies varied in a similar manner to the number of mummies. Thus, the species of aphid-attending ant determines the seasonal difference in the abundance of the ant-adapted parasitoid in ant-attended aphid colonies. Possible underlying mechanisms for this result and its implications for the biological control of ant-attended aphids on citrus are discussed.

Does urbanization explain differences in interactions between an insect herbivore and its natural enemies and mutualists?

Urbanization can alter the composition of arthropod communities. However, little is known about how urbanization affects ecological interactions. Using experimental colonies of the black bean aphid Aphis fabae Scopoli reared on Vicia faba L, we asked if patterns of predator-prey, host-parasitoid and ant-aphid mutualisms varied along an urbanization gradient across a large town in southern England. We recorded the presence of naturally occurring predators, parasitoid wasps and mutualistic ants together with aphid abundance. We examined how biotic (green areas and plant richness) and abiotic features (impervious surfaces and distance to town center) affected (1) aphid colony size, (2) the likelihood of finding predators, mutualistic ants and aphid mummies (indicating the presence of parasitoids), and (3) how the interplay among these factors affected patterns of parasitoid attack, predator abundance, mutualistic interactions and aphid abundance. Aphid abundance was best explained by the number of mutualistic ants attending the colonies. Aphid predators responded negatively to both the proportion of impervious surfaces and to the number of mutualistic ants farming the colonies, and positively to aphid population size, whereas parasitized aphids were found in colonies with higher numbers of aphids and ants. The number of mutualistic ants attending was positively associated with aphid colony size and negatively with the number of aphid predators. Our findings suggest that for insect-natural enemy interactions, urbanization may affect some groups, while not influencing others, and that local effects (mutualists, host plant presence) will also be key determinants of how urban ecological communities are formed.

Eficacia de insecticidas botánicos sobre <i>Myzus persicae</i> (Sulzer) y <i>Aphis gossypii</i> (Clover) (Hemiptera: Aphidiae) en el cultivo de pimiento (<i>Capsicum annuum</i> L.) bajo cubierta

Una gran variedad de artrópodos plaga causan, a nivel mundial, perjuicios en cultivos hortícolas. Myzus persicae (Sulzer), Aphis gossypii (Glover) (Hemiptera: Aphididae) son las principales plagas de artrópodos que afectan a cultivos de pimiento bajo cubierta. El propósito de este estudio fue determinar la efectividad de cuatro productos botánicos diferentes como una alternativa ecológica para el control de pulgones en cultivo protegido de pimiento en Concordia, Argentina. Se probaron formulaciones de extractos/aceites vegetales a base de: aceite esencial de canela Cinnamomun verum (J. Presl.) [AE canela]; aceite esencial de cuasia Quassia amara (L.) [AE cuasia], aceite de neem Azadarichta indica (A. Juss.) [M neem] y extracto de ajo Allium sativum (L.) [M ajo]. Cabe aclarar que éstos dos últimos contienen a su vez otros extractos/aceites esenciales que fueron comparados con un testigo absoluto (agua). Se realizó una distribución de acuerdo con un diseño totalmente aleatorio con tres repeticiones. Los tratamientos se aplicaron directamente sobre el follaje con mochila manual iniciándose 1 semana después del trasplante y luego, semanalmente, hasta finalizar el ensayo. Posteriormente, se evaluó el número promedio total de pulgones por hoja. Estos resultados mostraron que el tratamiento con aceite de neem (en mezcla M neem) registró un número de pulgones menor comparado con el resto de los tratamientos y testigo absoluto. Sin embargo, el mayor número de pulgones parasitados (momias) fue observado en las hojas tratadas con el aceite esencial de cuasia (AE cuasia).