Showing papers by "Nicolas Desneux published in 2020"

Long-term and large-scale releases of Trichogramma promote pesticide decrease in maize in northeastern China

Abstract: The Asian corn borer, Ostrinia furnacalis , is one of the most important pests of corn crops in Northern China. From 2004 to 2015, a public financial support to biological control of the corn borer resulted in a significant increase in the cultivated area treated with Trichogramma dendrolimi parasitoid applications in corn field in the Jilin Province, in northeastern China. In the present study, we analyzed the impact of these parasitoid releases, from 2000 to 2015 in the Jilin province, on the control of the corn borer as well as on pesticide use. We demonstrated that the widespread large-scale use of T. dendrolimi applications against the Asian corn borer, while being effective for controlling the pest and ensuring competitive corn yields, led to a decrease in insecticide use across the province. The use of Trichogramma is an economically and competitive alternative to insecticide applications in northeastern China.

Phenolic monoterpene-rich essential oils from Apiaceae and Lamiaceae species: insecticidal activity and safety evaluation on non-target earthworms

Abstract: The genera Oliveria (Apiaceae), Thymus and Satureja (Lamiaceae) encompass important medicinal and aromatic plants of Iran, which contains noteworthy amounts of essential oils (EOs) that are worthy of exploitation on an industrial level, including pesticide formulation development. In this study, the efficacy of five EOs obtained from O. decumbens, T. daenensis, S. sahendica, S. khuzistanica and S. rechingeri , was evaluated against three insects of economic relevance, the mosquito Culex quiquefasciatus , the housefly Musca domestica, and the moth Spodoptera littoralis . Potential non-target effects of these EOs were assessed on earthworms, Eisenia fetida . The chemical composition of the five EOs was determined by gas chromatography (GC-FID) and gas chromatography-mass spectrometry (GC-MS). EOs from O. decumbens, T. daenensis, S. khuzistanica and S. rechingeri were characterized by oxygenated monoterpenes (70.3, 91.6, 89.7 and 89.4%, respectively), whereas the EO from S. sahendica was dominated by monoterpene hydrocarbons (63.3%) followed by oxygenated monoterpenes (35.3%). In all cases, the biogenetically related thymol (0.3–36.7%), carvacrol (1.3–89.6%), p -cymene (2.1–13.7%) and γ-terpinene (1.5–41.3%) were found as the characteristic volatile compounds of the five EOs, with high quantitative variation according to the species considered. The five EOs exhibited high toxicity on the three target insects, with LC 50 /LD 50 values in the range of 16.2–29.3 µg mL -1 , 18.1–48.1 µg adult -1 and 7.4–23.1 µg larva -1 on C. quinquefasciatus, M. domestica and S. littoralis , respectively. Toxicity of the five EOs on non-target soil invertebrates was minimal, leading to no or very low (5.0–7.5%) mortality on E. fetida when tested at the concentration of 200 mg kg -1 , at variance with the positive control α-cypermetrin, which caused 100% mortality at 0.1 mg kg -1 of soil. Overall, our study discloses new opportunities to farmers growing these Iranian endemic plants, shedding light on the potential of these EOs to formulate effective and eco-friendly insecticides.

Fitness costs in chlorfenapyr-resistant populations of the chive maggot, Bradysia odoriphaga

Abstract: The chive maggot, Bradysia odoriphaga (Yang and Zhang) is an economically important insect pest, affecting many key vegetables, including Chinese chive, especially in northern China. Chlorfenapyr, a halogenated pyrrole insecticide that interferes with mitochondrial oxidative phosphorylation is widely used against B. odoriphaga. In this study, we evaluated selection-induced resistance to chlorfenapyr and fitness costs in B. odoriphaga. The results showed that B. odoriphaga developed 43.32-fold resistance after continuous exposure to chlorfenapyr for over 10 consecutive generations. The life-history traits of chlorfenapyr-resistant and susceptible strains were compared using age-stage, two-sex life table approach. No significant effects were observed on the longevity and pre-adult period. However, reduction in the total pre-oviposition period (TPOP) and fecundity (eggs/female) were observed in the resistant strain. Moreover, the demographic parameters such as intrinsic rate of increase (r), net reproductive rate (R0) and finite rate of increase (λ) were also decreased significantly in the resistant strain compared to the susceptible strain. These results showed the potential of B. odoriphaga to develop resistance against chlorfenapyr under continuous selection pressure. Furthermore, there was a fitness cost linked with chlorfenapyr resistance in B. odoriphaga. We conclude that a better knowlegde on the trade-off at play between resistance degree and fitness cost could be crucial for developing further management of B. odoriphaga in China.

Effect of crop diversity on predation activity and population dynamics of the mirid predator Nesidiocoris tenuis

Abstract: A considerable body of evidence has demonstrated the positive impact of the diversity of plant species on biological control of pests at the field scale. However, very few studies have assessed the effect of crop diversity on natural enemy performance and pest control. In order to test our hypothesis that crop diversity could increase natural enemy development and performance, we examined the mechanisms underlying the effect of two types of crop succession, i.e., multiple-crop succession (tomato, squash and soybean) and mono-crop succession (each crop alone), on population dynamics, predation capacity and spillover of Nesidiocoris tenuis Reuter (Hemiptera: Miridae) in a greenhouse experiment. We found that (1) the polyculture supported lower population growth of N. tenuis and lower predation rates of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) eggs compared to tomato and squash monocultures, but that correspondingly (2) the predator performed better on the polyculture than on the soybean monoculture. These results revealed that crop identity within the succession is a major factor in determining population dynamics and biological control. We found that compared to soybean monoculture, the presence of soybean Glycine max L. (Fabales: Fabaceae) in the polyculture treatment reduced the population dynamics of the mirid predator but increased biological control. This result suggests that non-host crops in a polycultural succession could benefit from the natural enemy populations that were increased by other suitable crops in the succession.

Highly diversified crop systems can promote the dispersal and foraging activity of the generalist predator Harmonia axyridis

Abstract: High plant biodiversity and landscape food provision stability is known to have a positive impact on biocontrol services provided by natural enemies. However, few studies have assessed how differential spatial and temporal crop richness actually impact biocontrol services, and notably how natural enemies may spill-over among crops. Within this framework, using a four-cage maze system under laboratory conditions, we evaluated the effect of a diversified crop system (four crops, namely cotton, tomato, squash and soybean) and low diversified crop systems (one single crop), on the generalist predator Harmonia axyridis (Pallas) and its predation capacity on aphids. The system varied food availability both in space, i.e. different cages, and in time, i.e. different dates of resources implementation. In general, the effects of crops on the natural enemies’ traits observed in the diversified crop system resulted from the average effects of the individual low diversified crop systems; the impact of the predator was highly dependent on the plant. Low diversified crop systems actually proved to be either very suitable for the predator’s development (tomato and squash), or not at all (soybean and cotton), but inversely suitable in reducing pest population with lower efficacy in tomato and squash and higher efficacy in soybean and cotton. The spillover of the ladybird was strongest in the squash low diversified crop system and lowest in the cotton one, other systems showing intermediate spillover values. In the diversified crop system, the ladybird presence was always closely related to plant presence, and aphid populations were maintained at a stable population increase. Still, the predator was also found in cages lacking plants, as opposed to the low diversified crop systems; this hinted at the potential of the highly diversified crop system to promote ladybird dispersal and increase foraging activity. We demonstrate that increasing crop diversity in agroecosystems may help promote biocontrol services provided by H. axyridis by promoting its spillover between crops (e.g. while the plants are senescing and/or when they are harvested).

The outbreaks of nontarget mirid bugs promote arthropod pest suppression in Bt cotton agroecosystems.

Abstract: The adoption of Bt (Bacillus thuringiensis) crops has improved crop yield, reduced chemical insecticide use, and induced an increase in farmer profits; however, some concerns persist about their potential environmental risks, including the impact on nontarget arthropods (Romeis et al., 2008). In China, Bt cotton was first grown commercially in 1997. As the levels of cultivated Bt cotton increased, populations of the target pest Helicoverpa armigera were found to have substantially declined (Wu et al., 2008). In addition, reduced insecticide use in Bt cotton has shown positive side effects, such as increased pest biocontrol services provided by natural enemies (Lu et al., 2012), but also negative side effects, such as mirid bug outbreaks (Lu et al., 2010). How this shift in pest status may impact interspecific arthropod interactions in Bt cotton needs to be further investigated (Zeilinger et al., 2011; Hagenbucher et al., 2013; Zhang et al., 2018). Mirid bug feeding often causes tattered leaves on host plants, suggesting that interspecific competition with other leaf-feeding insects may occur. Furthermore, mirid bugs may also prey on the cotton aphid Aphis gossypii and other arthropod pests (Jiang et al., 2015). Hence, mirid bugs have the potential to act as arthropod biocontrol agents during their outbreaks. This article is protected by copyright. All rights reserved.

Impact of Trichogramma parasitoid age on the outcome of multiparasitism in the factitious host eggs of Chinese oak silkworm, Antheraea pernyi

Abstract: The age of Trichogramma parasitoids could influence biological traits which are of great importance for effectiveness of mass rearing systems Recent studies demonstrated that Trichogramma ostriniae (TO) could parasitize Antheraea pernyi eggs through multiparasitism along with other Trichogramma species, although few adults could emerge successfully It is important to characterize the factors modulating the performance of TO on A pernyi eggs, notably in order to try enhancing its quantitative emergence through multiparasitism for further use in biological control In this context, irrespective of host age, we tested different ages of TO females (from 05-day- to 6-day-old postemergence) in multiparasitism with Trichogramma chilonis (TC) on A pernyi eggs The results of the present study confirmed that TO parasitism on A pernyi eggs was largely age dependent Higher percentage of multiparasitism and higher number of emerged TO adults were recorded in the treatment where 3-day-old TO females were used for parasitization with TC on A pernyi host In addition, we also tested different female ratios of both Trichogramma species to find out an optimal ratio for use in mass production The highest percentage of multiparasitism, emergence and optimum emerged number of TO (per A pernyi egg) was observed with the ratio 3:2 (TO:TC) per 1 host egg This study demonstrated that the age of TO females can significantly affect their performance in multiparasitism of large A pernyi eggs These results prompt for more research in order to develop an effective multiparasitism-based production of TO at the industrial scale

Detrimental sublethal effects hamper the effective use of natural and chemical pesticides in combination with a key natural enemy of Bemisia tabaci on tomato.

Abstract: Background Bemisia tabaci(Hemiptera: Aleyrodidae) represents one of the greatest threats to agricultural crops. Chemical control is the primary tool used in integrated pest management (IPM) programs. However, release of the predatorNesidiocoris tenuis(Hemiptera: Miridae) on tomato plants is a highly recommended control tactic. The objective of this study was to evaluate the efficacy of a commercial borax plus citrus oil (BCO) product againstB. tabaciin the presence and absence ofN. tenuis. The synthetic insecticide lambda-cyhalothrin was used as a positive control. We also evaluated the sublethal effects of BCO on the behavior and predation rate ofN. tenuis. Results Our results demonstrated that BCO, alone and at its maximum recommended field rate forB. tabaci, was not effective in controlling the pest under laboratory conditions. Application of BCO simultaneous withN. tenuisrelease did not reduce the increase in theB. tabacipopulation. Effective control ofB. tabaciwas achieved using onlyN. tenuis. However, synthetic lambda-cyhalothrin pyrethroid, used here as a control, caused high pest mortality and led to on-site extinction ofN. tenuis, which did not occur for insects exposed to BCO. Lambda-cyhalothrin and BCO significantly affected the foraging behavior ofN. tenuis, reducing the predation rate, especially following exposure to lambda-cyhalothrin. Conclusion The insecticide lambda-cyhalothrin achieved satisfactory results in suppressingB. tabaci, but was harmful toN. tenuis. Additionally, lambda-cyhalothrin and BCO affected predator behavior.

Fitness costs in clothianidin-resistant population of the melon aphid, Aphis gossypii.

Abstract: Clothianidin is a second-generation neonicotinoid insecticide, widely used against sap-sucking insect pest including melon aphid, Aphis gossypii Glover (Hemiptera: Aphididae). This pest causes severe economic damage to Cucurbitaceae plants worldwide. In this study, we investigated clothianidin resistance development under continuous selection pressure. Moreover, the age-stage, two-sex life table approach was used to evaluate the impact of clothianidin resistance on the fitness of A. gossypii. A clothianidin resistant strain (CT-R) with a 23.17-fold resistance level was developed from a susceptible strain (CT-S) after continuous selection for 24 generations. Life table results showed a significant reduction in the relative fitness (0.847) of CT-R strain compared to the CT-S strain of A. gossypii. The developmental duration, oviposition days, total pre-oviposition period (TPOP), longevity, and fecundity of CT-R strain were found to be significantly lower when compared to CT-S strain. The demographic parameters, including the intrinsic rate of increase (r), finite rate of increase (λ), net reproductive rate (R0), and mean generation time (T) were also significantly decreased in CT-R strain compared to the CT-S strain. Both the reproductive and survival rates were affected by clothianidin resistance in CT-R strain compared with the CT-S strain of A. gossypii. Overall, our results demonstrate that in-depth knowledge about the trade-off at play between resistance degree and fitness cost might be useful to design resistance management strategies against A. gossypii.

Parasitism performance of the parasitoid Trichogrammadendrolimi on the plum fruit moth Grapholitha funebrana

Abstract: The egg parasitoid Trichogramma dendrolimi Matsumura is one of the most widely used agents in sustainable crop protection to manage many lepidopteran pests in China, especially via inundative releases. It has been used as an important biocontrol agent in Integrated Pest Management (IPM) programs for the control of the plum fruit moth Grapholitha funebrana Tr. However, accurate knowledge of the parasitoid’s biology and ecology is needed to optimize its practical application in pest management. In the current study, the effect of key factors on T. dendrolimi effectiveness as biocontrol agent, including host age, exposure time, parasitoid density and, host density was evaluated under laboratory conditions. The parasitoid showed a higher parasitism rate on younger over older G. funebrana eggs. When host egg density increased, the number of eggs parasitized by the parasitoid also increased, but parasitism rates decreased. The functional response of T. dendrolimi on G. funebrana eggs fitted the Holling type II Model ( N t = 0.932 N /(1+0.112 N )). When parasitoid density and exposure time of hosts to parasitoids increased, the parasitism rate of T. dendrolimi also increased. In addition, previous exposure of host eggs to ultraviolet (UV) light did not affect parasitism rate. All aforementioned factors did not influence the emergence rate of the parasitoid offspring. Our results would provide references for optimizing the application of T. dendrolimi inundative releases in large-scale management of G. funebrana in orchards.

Impact of a shared sugar food source on biological control of Tuta absoluta by the parasitoid Necremnus tutae

Abstract: Honeydew is a sugar-rich food source produced by sap-feeding insects, notably by major pests such as aphids and whiteflies. It is an important alternative food source for the adult stage of various key natural enemies (e.g., parasitoids), but it may be used also as food by agricultural pests. Necremnus tutae is an idiobiont parasitoid, and it is the most abundant larval parasitoid associated with the South American tomato pinworm, Tuta absoluta, in recently invaded European areas. The impact of N. tutae on T. absoluta populations was evaluated under greenhouse conditions with and without the presence of a honeydew producer, the aphid Macrosiphum euphorbiae. In addition, laboratory experiments were performed to evaluate the longevity of N. tutae and T. absoluta adults when fed with water, honey or honeydew produced by the aphid. In the greenhouse, N. tutae effectively reduced T. absoluta population by the end of the experiment, and this independently of the presence of the aphid; still the presence of M. euphorbiae led to delayed and reduced T. absoluta population peak when controlled by the parasitoid (there was a fourfold increase in parasitoid density in presence of aphid). The longevity of both N. tutae and T. absoluta females increased in the presence of honeydew (when compared to water only) under laboratory conditions; it hinted that honeydew could be used by an herbivore as T. absoluta. The interactions between the two phytophagous species showed contrasting effects, and this mostly independently of parasitoid presence. Tuta absoluta had no impact on aphid population dynamics. By contrast, the production of T. absoluta larvae was higher in the first part of the experiment as the adults lived longer (feeding on aphid honeydew) and produced more larvae. In the second part of the experiment, there were fewer T. absoluta larvae in the presence of the aphid, likely owing to resource competition and/or negative plant-mediated indirect interactions. We demonstrated that honeydew producers could impact parasitoid-host population dynamics both through direct and indirect interactions and that potential positive effects of a sugar food source toward a pest can be nullified in the long term by other negative effects occurring simultaneously.

Suitability of Chinese oak silkworm eggs for the multigenerational rearing of the parasitoid Trichogramma leucaniae.

Abstract: Trichogramma leucaniae is believed to be an efficient biological control agent for controlling the soybean pod borer [SPB; Leguminivora glycinivorella]. The large eggs of Chinese oak silkworm, Antheraea pernyi, are one of the best alternative host for mass production of Trichogramma. However, they are considered poor host for the growth and development of T. leucaniae. Here, we determine the feasibility of successive rearings of T. leucaniae on the large eggs for eight generations and evaluated their capacity of parasitizing SPB eggs of different ages. In the first four generations, the suitability of T. leucaniae reared on large eggs exhibited a significant increasing tendency and then decreased with the successive generations thereafter. The percentage of parasitized eggs and number of emerged adults per egg were increased from 40.0% and 10.8 adults/egg in F1 generation to 86.7% and 36.4 adults/egg in F4 generation respectively. In addition, T. leucaniae reared on A. pernyi for four generations significantly parasitized more SPB eggs regardless of egg age compared with those reared on Corcyra cephalonica eggs. These results provided useful information on the feasibility of mass production of T. leucaniae by reared for successive generations on A. pernyi large eggs.

Effects of Aphid Density and Plant Taxa on Predatory Ladybeetle Abundance at Field and Landscape Scales

Abstract: In agroecosystems, predatory ladybeetles play an important role in restraining aphid population growth and suppressing aphid populations. They can adapt to various habitats and make use of various aphid species associated with multiple host plants during their life cycle. Agricultural landscapes in China are composed of a mosaic of small fields with a diverse range of crops, and how ladybeetles make use of host plant diversity in such landscapes has rarely been documented. In this study, we examined the relationship between aphid densities and ladybeetle densities in two different settings: (i) on the majority of plant species (including crops, trees, and weeds) at a local field scale in 2013 and 2014, and (ii) in paired cotton and maize crop fields at a regional landscape scale in 2013. Overall, we found that aphid abundance determined predatory ladybeetle abundance at both the local field and landscape scales, and there was a positive correlation between aphid densities and ladybeetle densities. However, plant taxa had no significant influence on the predatory ladybeetle abundance at the local field scale. In addition, the effect of aphids on ladybeetles abundance was influenced by the crop type and growing season at the regional landscape scale. There was a significant positive correlation between aphids and ladybeetles populations on cotton only in July and August, whereas the correlation was significant for maize throughout the whole growing season. We also conducted an analysis of the stable carbon isotope ratios of the adult ladybeetles caught in cotton and maize fields (C3 and C4 crops, respectively) in a regional landscape-scale survey in 2013. The δ13Cvalue indicated that most prey aphids for ladybeetles originated from crops where aphids are abundant (cotton in June and July; both maize and cotton in August).These findings improved our understanding of the migration and dispersal of ladybeetles among different habitats and plant species and provided insight into the promotion of the regional conservation and pest control of natural enemies in northern China.

Impact of heat stress on the development of egg and adult coccinellid Serangium japonicum : evidence for cross-stage and cross-generation effects

Abstract: Arthropod biological control agents are at risk due to climate change, since heat stress negatively impacts their life history traits. Here, we investigated ontogenetic variation of thermal sensitivity in an important whitefly predator, Serangium japonicum Chapin (Coleoptera: Coccinellidae). In particular, we evaluated the impact of heat shock on survival rate, development, and reproduction of S. japonicum , and checked whether the negative effects resulting from heat stress are stage-related. The two most heat-tolerant stages of S. japonicum (egg and adult) were exposed to heat shock treatments at 36, 39, and 42 oC for 2 h, and 36 and 39 oC for 4 h. We found that heat shock significantly reduced egg-to-adult survival rate, extended egg-to-adult development time, and decreased fecundity and oviposition period compared to control (27 oC). The sex ratio however was not affected. Eggs exposed to heat shock led to adults whose weight and longevity were considerably reduced. The detrimental effects that resulted from heat shock were carried over to later life stages and even the next generation. Those carry-over effects were independent of stage except for egg-to-adult development time and adult weight. Our results suggest that releasing eggs or adults into fields or greenhouses makes little difference in reducing any negative impact on the developmental performance of S. japonicum induced by heat stress in a warming climate.

Hosting certain facultative symbionts modulate the phenoloxidase activity and immune response of the pea aphid Acyrthosiphon pisum

Abstract: The pea aphid Acyrthosiphon pisum hosts different facultative symbionts (FS) which provide it with various benefits, such as tolerance to heat or protection against natural enemies (e.g. fungi, parasitoid wasps). Here, we investigated whether and how the presence of certain FS could affect phenoloxidase activity, a key component of insect innate immunity, under normal and stressed conditions. For this, we used clones of A. pisum of different genetic backgrounds (LL01, YR2 and T3-8V1) lacking FS or harboring one or two (Regiella insecticola, Hamiltonella defensa, Serratia symbiotica + Rickettsiella viridis). Gene expression and proteomics analyses of the aphid hemolymph indicated that the two A. pisum phenoloxidases, PPO1 and PPO2, are expressed and translated into proteins. The level of PPO genes expression as well as the amount of PPO proteins and phenoloxidase activity in the hemolymph depended on both the aphid genotype and FS species. In particular, H. defensa and R. insecticola, but not S. symbiotica + R. viridis, caused a sharp decrease in PO activity by interfering with both transcription and translation. The microinjection of different types of stressors (yeast, Escherichia coli, latex beads) in the YR2 lines hosting different symbionts affected the survival rate of aphids and, in most cases, also decreased the expression of PPO genes after 24 h. The amount and activity of PPO proteins varied according to the type of FS and stressor, without clear corresponding changes in gene expression. These data demonstrate that the presence of certain facultative symbionts influences an important component of pea aphid immunity. This article is protected by copyright. All rights reserved.

Insects in agroecosystems – an introduction

Abstract: Agroecology is the study of linkages in agricultural systems and it derives from the need to understand and restore natural connections and ecological complexity to control insect and other pest populations. The present special issue addresses a rich variety of agroecosystems spanning the globe, involving the roles of a range of insects on a great many crops. The overview will further improve our understanding of the complex ecology of the players and the ecological complexity of the crop systems.

Water and salt stresses do not trigger bottom-up effects on plant-mediated indirect interactions between a leaf chewer and a sap-feeder

Abstract: Soil abiotic stresses can trigger bottom-up effects on insect pests However, it remains unknown whether the bottom-up effects differentially affect leaf chewers and sap-feeders, and whether abiotic stresses alter the extent of indirect interactions between insect herbivores sharing a host plant We carried out a set of manipulative experiments to investigate how abiotic and biotic stresses affected performance associated with insect herbivory (eating by leaf chewer or sap-feeder) and plant physiological conditions (manipulating water and/or salt inputs) We examined the performance of response species (sap-feeder Macrosiphum euphorbiae and leaf chewer Tuta absoluta) on tomato plants Solanum lycopersicum that were exposed to eight conditions in a full factorial design based on (1) optimal or limited water inputs, (2) with or without 100 mM NaCl, and (3) with or without pre-infestation by insect herbivors showing distinct feeding habit Water and salt stresses slowed down plant growth in terms of plant height and node number, which subsequently negatively affected the herbivores via bottom-up effects Tuta absoluta larval development was adversely affected by water limitation, while M euphorhiae survival and fertility were adversely affected by salinity stress After pre-infestation by the inducing species (ie feeding activity on the plant), the test species (either M euphorbiae or T absoluta) exhibited a lower performance, that is, lower M euphorbiae survival and fewer offspring, and extended T absoluta developmental duration and reduced pupal weight These results suggested an apparent competition between the herbivores; however, neither water limitation nor salt stress affected the magnitude of the negative indirect interactions between the two insect species Our findings shed light on how cascading force(s) and induced indirect resistance(s) could be used to improve integrated pest management programs

An increased risk of parasitism mediated by the facultative symbiont Regiella insecticola

Abstract: Previous data showed that the parasitoid wasp Aphelinus asychis was more successful on Sitobion avenae clones artificially infected with different strains of Regiella insecticola compared to the same clones lacking facultative symbionts. To test whether this resulted from a specific interaction between the aphid and symbiont genotype, we used new clonal lines from a different genotype of S. avenae (Linyi) infected with the same R. insecticola strains. The parasitism rate of A. asychis was higher on the two Linyi lines infected with R. insecticola than on the uninfected control line, while the emergence rate was lower due to higher mortality during development. However, a different wasp species, Aphidius gifuensis, showed no difference in the parasitism rate and emergence rate between the three Linyi lines, suggesting that the increase in parasitism rate could be wasp species-dependent. The mortality of A. asychis during development in the presence of R. insecticola may be linked to (i) a direct toxic or metabolic effect since the weight of the emerged wasps was also reduced and (ii) a general effect on the aphid fitness since the survival and fecundity of infected aphids having survived A. asychis attack were clearly reduced compared to the control, while those surviving A. gifuensis attack had only a slight increase in their survival rate. Our data therefore enriched the panel of phenotypic effects that R. insecticola could contribute to the aphid and emphasized the potential implications of symbionts on biological pest control.