Host instar suitability of Aphis gossypii (Hemiptera: Aphididae) for Lysiphlebus testaceipes (Hymenoptera: Braconidae) and parasitism effect on aphid life table

Lysiphlebus testaceipes (Cresson) (Hymenoptera: Braconidae, Aphidiinae) has constituted a well-studied parasitoid insect model, but very little is known about the host-instar suitability of aphid for the wasp so far. One of the hosts of L. testaceipes is Aphis gossypii Glover (Hemiptera: Aphididae). The latter is a serious aphid pest to vegetable production in Benin. Therefore, the objectives of our study were to: (1) examine the oviposition behavior of L. testaceipes on A. gossypii; (2) investigate the host-instar suitability of A. gossypii for L. testaceipes; and (3) compare the life table parameters of A. gossypii with aphids parasitized by L. testaceipes and unparasitized aphids (control). The study was conducted in a laboratory at 26 ± 1 °C in petri dishes and revealed that the parasitoid utilized up to seven stabbing stings to handle and oviposit, particularly in older A. gossypii. In aphids parasitized at the third instar, the net reproductive rate R _o as well as the intrinsic rate of natural increase r _m was significantly lower (2.119 ± 0.272 and 0.110 ± 0.018) compared to the control (15.529 ± 1.287 and 0.272 ± 0.008), respectively (p < 0.01).     

Aphid Honeydew Quality as a Food Source for Parasitoids Is Maintained in Bt Cotton

Bt-transgenic cotton has proven to be highly efficient in controlling key lepidopteran pests. One concern with the deployment of Bt cotton varieties is the potential proliferation of non-target pests. We previously showed that Bt cotton contained lower concentrations of insecticidal terpenoids as a result of reduced caterpillar damage, which benefited the aphid Aphis gossypii. It is thus important that non-target herbivores are under biological control in Bt cotton fields. The induction or lack of induction of terpenoids could also influence the quality of aphid honeydew, an important food source for beneficial insects. We therefore screened A. gossypii honeydew for cotton terpenoids, that are induced by caterpillars but not the aphids. We then tested the influence of induced insect-resistance of cotton on honeydew nutritional quality for the aphid parasitoid Lysiphlebus testaceipes and the whitefly parasitoid Eretmocerus eremicus. We detected the cotton terpenoids gossypol and hemigossypolone in A. gossypii honeydew. Although a feeding assay demonstrated that gossypol reduced the longevity of both parasitoid species in a non-linear, dose-dependent manner, the honeydew was capable of sustaining parasitoid longevity and reproduction. The level of caterpillar damage to Bt and non-Bt cotton had no impact on the quality of honeydew for the parasitoids.These results indicate that the nutritional quality of honeydew is maintained in Bt cotton and is not influenced by induced insect resistance.     

The potential host ranges in Australia of some imported aphid parasites [Hym: Ichneumonoidea: Aphidiidae]

Host selection trials on restricted populations of the aphidiid parasites,Lysiphlebus fabarum (Marshall) andL. testaceipes (Cresson), imported into Australia as biological control agents ofAphis craccivora Koch, the cowpea aphid, have shown that these imported parasites are not widely polyphagous, and thus support a view that the 2 species, as presently recognized, each represent a complex of host-restricted biotypes or of sibling species. Whereas both of the importedLysiphlebus readily oviposited in species ofAphis andToxoptera, and developed successfully to adulthood inA. craccivora, A. gossypii Glover andT. aurantii (Boyer de Fonscolombe), they failed to complete development inA. citricola van der Goot, one of the most common aphid species in Australia, and only a small number completed development inT. citricidus (Kirkaldy). Both of these hosts, then, act as “egg traps” for theLysiphlebus. A. nerii Boyer de Fonscolombe was a suitable host forL. testaceipes but not forL. fabarum. NeitherL. fabarum notL. testaceipes oviposited inCavariella aegopodii (Scopoli),Brevicoryne brassicae (L.),Brachycaudus helichrysi (Kaltenbach),B. persicae (Passerini),Hyperomyzus lactucae (L.),Acyrthosiphon kondoi Shinji,A. pisum (Harris),Macrosiphum euphorbiae (Thomas) orM. rosae (L.); andL. fabarum did not oviposit inRhopalosiphum padi (L.) orMyzus persicae (Sulzer). The prognosis for the effective establishment in Australia of these 2 parasites is therefore not good In contrast, another purportedly polyphagous aphidiid,Praon volucre (Haliday), imported into Australia to help effect control ofH. lactucae, the sowthistle aphid, successfully and effectively parasitizedMacrosiphum euphorbiae, M. rosae, Acyrthosiphon pisum, A. kondoi, Aulacorthum solani (Kaltenbach),Myzus persicae andAphis craccivora, in addition toH. lactucae.     

Indirect multi-trophic interactions mediated by induced plant resistance: impact of caterpillar feeding on aphid parasitoids

Cotton produces insecticidal terpenoids that are induced by tissue-feeding herbivores. Damage by Heliothis virescens caterpillars increases the terpenoid content, which reduces the abundance of aphids. This effect is not evident in Bt-transgenic cotton, which is resistant to H. virescens. We determined whether induction of terpenoids by caterpillars influences the host quality of Aphis gossypii for the parasitoid Lysiphlebus testaceipes and whether this interaction is influenced by Bt cotton. The exposure of parasitoids to terpenoids was determined by quantifying terpenoids in the aphids. We detected several terpenoids in aphids and found a positive relationship between their concentrations in plants and aphids. When L. testaceipes was allowed to parasitize aphids on Bt and non-Bt cotton that was infested or uninfested with H. virescens, fewer parasitoid mummies were found on infested non-Bt than on Bt cotton. Important parasitoid life-table parameters, however, were not influenced by induced resistance following H. virescens infestation, or the Bt trait. Our study provides an example of a tritrophic indirect interaction web, where organisms are indirectly linked through changes in plant metabolites.     

Differences in the high-temperature tolerance of <Emphasis Type="Italic">Aphis craccivora</Emphasis> (Hemiptera: Aphididae) on cotton and soybean: implications for ecological niche switching among hosts

To forecast the effects of climate change and extreme temperature events on insect population dynamics, the high-temperature tolerance of insects must be taken into account. We compared the life-history characteristics of cowpea aphid (Aphis craccivora Koch) across different temperature regimes on two different host plants, soybean (a preferred host) and cotton (a non-preferred host). Most demographic parameters were superior for the aphid on soybean than on cotton. Temperatures affected aphid development more on cotton than on soybean. The intrinsic rate of increase, reproduction rate, number of progeny per adult, and longevity were significantly higher on soybean than on cotton for the same temperature regime. Temperatures that fluctuated to extreme levels caused a rapid decline in each of these parameters for aphids fed on cotton, but not for those fed on soybean. To our knowledge, this is the first report to note that the high-temperature tolerance of A. craccivora is host-specific (cotton vs. soybean). Our findings may partly explain the observed niche switching of the cowpea aphid (Aphis craccivora) from cotton to soybean at the beginning of summer when the temperature goes up in the Xinjiang cotton-growing zone (Northwest China). This host mediation of high-temperature tolerance in aphids should be taken into account when modeling population dynamics under the influence of global warming, host adaptation, and the risk analysis of alien pest invasions.     

Lysiphlebus testaceipes,an introduced aphid parasitoid in portugal [Hym.: Aphidiidae]

Lysiphlebus testaceipes (Cresson), an exotic parasitoid species introduced in 1973–74 into southern France and subsequently widespread over the whole mediterranean France, Italy and Spain has become established even in Portugal since 1985. It was found on the southern coast of Portugal parasitizingAphis nerii Boyer de Fonscolombe. In 1986 it spread towards the North, its host range expanded and now includesAphis chloris Koch,Aphis citricola van der Goot,Aphis fabae Scopoli,Aphis frangulae Kaltenbach,Aphis gossypii Glover,A. nerii, Aphis parietariae Theobald,Aphis sedi Kaltenbach,Toxoptera aurantii (Boyer de Fonscolombe). The proved complete development and a high parasitization ofL. testaceipes onA. citricola is the 1st case in the whole Mediterranean, from where only incomplete development and a negligible percentage of parasitization (Italy) have been reported. Both the host range composition and development ofL. testaceipes indicate an increase of genetic polymorphism in the established populations. Interspecific relations ofL. testaceipes and the indigenous parasitoid species indicate an increasing dominance of the exotic biocontrol agent.      

Host range of a newly introduced parasitoid, Binodoxys communis among common aphid species in Hawaii

Binodoxys communis (Gahan) (Hymenoptera:Braconidae), a parasitoid of aphids originally from China, was introduced into Hawaii and evaluated in the laboratory for its ability to detect, accept, oviposit and develop in Aphis gossypii reared on two host plants, plus five other common aphid species. The parasitoid was able to detect all six aphid species and to successfully sting five species, with highest preference for those in the genus Aphis. Aphis species were highly suitable for parasitoid development. Other species were only marginally suitable. Parasitoids spent less time searching on plants of less acceptable aphids. Aphid defensive behaviors did not affect oviposition success, but did lengthen the parasitoid’s handling time of several aphid species. Host acceptance was positively correlated with host suitability, yet one unsuitable host was readily accepted for oviposition.     

The microbial flora of Aphis gossypii: Patterns across host plants and geographical space

The cotton aphid, Aphis gossypii, has a worldwide distribution and causes damage to numerous economically important crops. The bacterial symbionts associated with cotton aphids, sampled mainly from malvaceous and cucurbitaceous plants within Japan and Australia, were characterised using molecular profiling approaches. The goal was to document the aphid symbionts present and determine if patterns of microbial diversity are consistent with the existence of host plant related cryptic species in A. gossypii. The bacterial profiles of the aphids are diverse and reflect local geography more than host plant use.     

Foraging behaviour of the parasitoid Lysiphlebus testaceipes (Hymenoptera: Braconidae) in response to plant volatiles,with reference to biocontrol of aphids in peri-urban vegetable production systems

Foraging behaviour of Lysiphlebus testaceipes was studied in a Y-tube olfactometer. Naïve females responded to the Aphis gossypii/eggplant complex on which they had been reared, but did not show a preference for this aphid/plant complex over an uninfested eggplant, an eggplant that had been damaged by the aphid or an A. gossypii/okra complex. Females that had been allowed to forage on the A. gossypii/eggplant complex before being tested in the olfactometer showed a strong preference for an uninfested eggplant over an uninfested okra plant and for the A. gossypii/eggplant complex over an A. gossypii/okra complex, indicating that they had learned to associate eggplant-derived volatiles with host availability. When females that had been reared on the A. gossypii/eggplant complex were tested after foraging experience on the A. gossypii/okra complex, they did not show a preference for either complex, suggesting that they still retained a memory of the cues associated with the complex on which they had been reared. The efficiency of L. testaceipes as a biological control agent in peri-urban vegetable production, such as the Cuban organoponics system, potentially could be improved by producing and releasing females behaviourally primed to prefer specific host/plant complexes.     

The prospect of using sub-lethal imidacloprid or pirimicarb and a parasitoid wasp, Lysiphlebus fabarum, simultaneously,to control Aphis gossypii on cucumber plants

The broad-spectrum insecticides greatly influence the control of cotton aphids; however, due to frequent chemical control, Aphis gossypii (Hemiptera: Aphididae) has developed resistance against several classes of synthetic insecticides. In this study, we explored the sub-lethal effects of imidacloprid and pirimicarb, two commonly used insecticides for aphid control, on a parasitoid wasp, Lysiphlebus fabarum (Marshall) (Braconidae: Aphidiinae), when simultaneously used to control melon aphid on cucumber plants, as part of a comprehensive study for integrated pest management. Bioassays of imidacloprid and pirimicarb were performed to calculate LC₅₀ with third instars of A. gossypii. The LC₅₀ of these insecticides (110.55 and 250.89 μg/lit, respectively) were used to expose the wasp larvae, pupae, and adult parasitoids on a cucumber leaf. The percent mortality, percent adult emergence, and sex ratio were calculated during each exposure test. Moreover, the body size, egg load, and mature egg size of wasps surviving the insecticide treatments, as well as the sex ratio of the second generation was evaluated. Regardless of the host aphid mortality, none of the insecticides caused mortality of larval stage of the parasitoid. The insecticide application on pupal stage revealed that the percentage of mortality, sex ratio, body size, and egg load of surviving wasps, as well as the sex ratio of their offspring was adversely affected by imidacloprid, but not by pirimicarb. The present study suggests pirimicarb as a preferred insecticide, with less harmful effects on the fitness components of L. fabarum, for integrated pest management of cotton aphids.     

Prey species affects the performance of the aphidophagous ladybird,Coelophora saucia

Performance of ladybird, Coelophora saucia (Mulsant) was studied on seven aphid species in terms of various life attributes. Immature stages developed fastest and survived most on Aphis craccivora. Longevity, fecundity and egg fertility of adults were highest on A. craccivora. Age specific fecundity was triangular in shape with the occurrence of peak oviposition at an early age on A. craccivora and at a later age on Lipaphis erysimi. The net reproductive rate, intrinsic rate of increase, and finite rate of increase of C. saucia were highest on A. craccivora and lowest on L. erysimi. Owing to better performance of C. saucia on A. craccivora, this is considered as the most suitable prey followed by Myzus persicae, Aphis gossypii, Rhopalosiphum maidis, Ceratovacuna silvestrii, Aphis nerii and L. erysimi. It is the first attempt to evaluate prey suitability of this ladybird based on several attributes.     

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.     

Evaluation of four aphidiine parasitoids for biological control ofAphis gossypii

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

Density-dependent parasitism of cowpea aphid,Aphis craccivora by Lysiphlebus fabarum,Binodoxys acalephae,and Aphidius matricariae (Hymenoptera: Braconidae: Aphidiinae)

Biological control, as a major component of pest management strategies, uses natural biological agents to reduce pest populations. Studying the interaction among Aphis craccivora and its parasitoids including, Lysiphlebus fabarum, Binodoxys acalephae, and Aphidius matricariae in 2016 and 2017 in Tehran Parke-Shahr, showed positive, significant correlations in all cases between the densities of three parasitoid species and that of aphid nymphs and adults. The density of the parasitoids increased by increasing the density of the aphids. The parasitoids showed aggregative behavior in response to different densities of the host. There was a positive density-dependent correlation between the density of A. craccivora and rate of parasitism. Parasitism rates of nymphs and adult aphids by L. fabarum, B. acalephae, and A. matricariae increased or decreased along with decline or increase in the population of the aphid host. In 2016 spring, the highest rates of parasitism on aphid nymphs by L. fabarum, B. acalephae, and A. matricariae were 46.82, 23.09, and 17.16%, respectively. In 2017 spring, the highest rates of parasitism on aphid nymphs by L. fabarum, B. acalephae, and A. matricariae were 48.97, 21.77, and 15.06%, respectively. So, given the accordance between changes in aphid population and that of parasitoids, and parasitoids’ efficacy in Tehran’s polluted air, they can be used as biological agents in the management of A. craccivora population.     

Host‐associated differentiation and evidence for sexual reproduction in Iranian populations of the cotton aphid,Aphis gossypii

Phytophagous insects with wide host ranges often exhibit host‐associated genetic structure. We used microsatellite analysis to assess the population structure of the cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae), a serious pest on many economically important crops worldwide. We sampled aphids from five host plant species in Iran and detected strong population subdivision, with an overall multilocus F_ST of 0.191. The matrix of pairwise F_ST values indicated that differentiation between populations collected from different hosts was significantly stronger than between populations from the same hosts. Host‐associated differentiation was further supported by Bayesian clustering analyses, which grouped all samples from cotton together with aubergine, and all samples from cucumber together with pumpkin and hibiscus. This adds to the growing body of evidence that many seemingly generalist aphids are in fact an assemblage of host‐specialized lineages. Although we detected a clear genetic signature of clonal reproduction, the genotypic diversity of A. gossypii in Iran is much higher than in other parts of the world. Particularly samples from cotton exhibited a surprisingly high genotypic diversity, suggesting that many lineages on this host are cyclical parthenogens that engage in regular bouts of sexual reproduction.     

A defensive endosymbiont fails to protect aphids against the parasitoid community present in the field

1. The value of protective mutualisms provided by some facultative endosymbionts has been well demonstrated in the laboratory, yet only recently has their effectiveness in the field been studied. ‘Candidatus Hamiltonella defensa’ is known to defend aphids from parasitoid wasps in laboratory trials. However, the efficacy of this defence varies among parasitoids, suggesting that protection will vary spatially and temporally depending on parasitoid community composition. 2. This demonstrated specificity and a dearth of studies on Hamiltonella in the field prompted the authors to quantify parasitism rates of Hamiltonella‐infected and ‐uninfected Aphis craccivora Koch aphid colonies in a manipulative field study. 3. It was found that A. craccivora in central Kentucky alfalfa were parasitised by Lysiphlebus testaceipes (Cresson) and Aphelinus sp. Surprisingly, Hamiltonella infection did not lower successful parasitism by the naturally occurring parasitoid wasps. Whether Hamiltonella was effective against L. testaceipes was subsequently tested in a controlled laboratory assay, and no effect on parasitism rate was found. 4. This study emphasises the fact that defensive symbionts sometimes provide no tangible defensive benefits under field conditions, depending on parasitoid community composition. It is hypothesised that the protective mutualism may be beneficial in geographically localised areas. When the symbiosis is effective against a local parasitoid community, aphid clones may experience eruptive population growth and rapidly disperse across a large area, allowing spread to habitats with different parasitoid communities where the mutualism is an ineffective defence.     

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.     

Nymphal and adult performance of Apolygus lucorum (Hemiptera: Miridae) on a preferred host plant, mungbean Vigna radiata

Mungbean, Vigna radiata (L.) Wilczek, a preferred host plant of Apolygus lucorum (Meyer-Dür) (Hemiptera: Miridae), is used in China as a trap crop for this pest in cotton fields. Little is known, though, about the relationship between adult oviposition preference and offspring performance of A. lucorum on mungbean. In this study, we compared the oviposition preference of A. lucorum on mungbean versus cotton plants in both open-field plots and field cages. Field-plot experiments demonstrated that the population density of first instar nymphs of A. lucorum and the ratio of first instar nymphs to adults were significantly higher on mungbean than on cotton. Choice and no-choice cage experiments revealed that the number of eggs laid on mungbean was significantly higher than on cotton. We also compared adult longevity and fecundity, as well as offspring survival and development on these two host plants. We found that A. lucorum adult females survived longer and laid more eggs on mungbean than on cotton (P?<?0.05). Mungbean also promoted higher rates of development than did cotton (P?<?0.05), but did not affect nymphal survival (P?>?0.05). In summary, the preference of A. lucorum adults for mungbean is consistent with both adult and nymphal performance. This study furthers the understanding of the relationship between the polyphagous species A. lucorum and its host plants, which will help improve trap-cropping strategies for the control of A. lucorum that are based on the use of mungbean.     

Effects of elevated CO2 and plant genotype on interactions among cotton,aphids and parasitoids

Abstract Effects of CO₂ level (ambient vs. elevated) on the interactions among three cotton (Gossypium hirsutum) genotypes, the cotton aphid (Aphis gossypii Glover), and its hymenoptera parasitoid (Lysiphlebia japonica Ashrnead) were quantified. It was hypothesized that aphid‐parasitoid interactions in crop systems may be altered by elevated CO₂, and that the degree of change is influenced by plant genotype. The cotton genotypes had high (M9101), medium (HZ401) and low (ZMS13) gossypol contents, and the response to elevated CO₂ was genotype‐specific. Elevated CO₂ increased the ratio of total non‐structural carbohydrates to nitrogen (TNC: N) in the high‐gossypol genotype and the medium‐gossypol genotype. For all three genotypes, elevated CO₂ had no effect on concentrations of gossypol and condensed tannins. A. gossypii fitness declined when aphids were reared on the high‐gossypol genotype versus the low‐gossypol genotype under elevated CO₂. Furthermore, elevated CO₂ decreased the developmental time of L. japonica associated with the high‐gossypol genotype and the low‐gossypol genotype, but did not affect parasitism or emergence rates. Our study suggests that the abundance of A. gossypii on cotton will not be directly affected by increases in atmospheric CO₂. We speculate that A. gossypii may diminish in pest status in elevated CO₂ and high‐gossypol genotype environments because of reduced fitness to the high‐gossypol genotype and shorter developmental time of L. japonica.