Aphelinus albipodus(Hymenoptera: Aphelinidae) andDiaeretiella rapae(Hymenoptera: Braconidae) Parasitism onDiuraphis noxia(Homoptera: Aphididae) Infesting Barley Plants Differing in Plant Resistance to Aphids

Russian wheat aphid,Diuraphis noxia(Mordvilko), as a pest of small grains, has prompted research into biological control and host plant resistance. In the presence of Russian wheat aphid, leaves of a susceptible barley (Morex) are curled and chlorotic and sustain large densities of this aphid, while leaves of a resistant barley (STARS-9301B) remain flat and green and sustain fewer aphids. Might parasitism of Russian wheat aphid byAphelinus albipodusHayat & Fatima andDiaeretiella rapaeMcIntosh be affected differently by these plant types? When presented the plants separately and based on parasitism rate relative to aphid density, the largerD. rapaewas more effective in parasitizing relatively high densities of aphids within curled leaves of Morex than relatively low densities of aphids on uncurled leaves of STARS-9301B. Parasitism byA. albipodusdid not significantly differ among the plants. When given a choice of plants, approximately equal rates of parasitism occurred on the two plant lines for both parasitoid species, and parasitism byD. rapaewas greater thanA. albipodus.These data indicate that using parasitoid size as an indicator of success in a physically restricted environment may be misleading, when considered in a plant environment responsive in several manners to aphids (chlorosis, curling, and ability to sustain Russian wheat aphid). We expect that use of resistant barley will result in decreased parasitoid abundance as aphid densities decrease. However, parasitism rates are expected to be approximately equal on resistant and susceptible barley. In this system, plant resistance and biocontrol are compatible management strategies.     

Effect of wheat resistance, the parasitoid Aphidius rhopalosiphi, and the entomopathogenic fungus Pandora neoaphidis, on population dynamics of the cereal aphid Sitobion avenae

The influence of wheat (Triticum aestivumL.) resistance, the parasitoid Aphidius rhopalosiphiDe Stephani-Perez (Hymenoptera: Braconidae) and the entomopathogenic fungus Pandora neoaphidis(Remaudière et Hennebert) Humber (Zygomycetes: Entomophthorales) on the density and population growth rate of the cereal aphid Sitobion avenae(F.) (Hemiptera: Aphididae) was studied under laboratory conditions. Partial wheat resistance was based on hydroxamic acids, a family of secondary metabolites characteristic of several cultivated cereals. The partial resistance of wheat cultivar Naofén, the action of the parasitoid and the joint action of the parasitoid and fungus, reduced aphid density. The lowest aphid densities were obtained with the combination of the parasitoid and the fungus, but wheat resistance under these circumstances did not improve aphid control. Significant reductions of population growth rate (PGR) of aphids were obtained with the joint action of wheat resistance and natural enemies. In particular, the combined effects of parasitoids and fungi showed significantly lower PGR than the control without natural enemies in both wheat cultivars. Our results support the hypothesis that wheat resistance and the utilization of biological control agents could be complementary strategies in an integrated pest management program against cereal aphids.     

Interactions betweenAcyrthosiphon kondoi [Homoptera: Aphidoidea] andAphelinus asychis [Hymenoptera: Chalcidoidea] and other parasites and hosts

In laboratory trials to investigate the parasite/host spectra of certain aphid pests and hymenopterous parasites, the aphidAcyrthosiphon kondoi Shinji encapsulated the egg of the aphelinid parasiteAphelinus asychis Walker. The resultant brown, sclerotic capsule was formed within 24 h of exposure of the aphid to parasitization and as far as is known prevented the development of the parasite to the larval stage. The capsule remained throughout the life of the aphid, whose longevity and fecundity were apparently not seriously impaired. A small number ofAphelinus escaped encapsulation, especially in aphids already containing capsule(s), and developed into normal, reproductive adults.A. kondoi did not encapsulate, andA. asychis was not encapsulated by any other species. However, thoughA. asychis readily parasitizedAphis citricola van der Goot,A. nerii Boyer de Fonscolombe andToxoptera citricidus (Kirkaldy), most of its progeny ceased development in these aphids before reaching the mummification stage, and died within the dead or dying, non-mummified aphid host.     

Hydroxamic acids affecting barley yellow dwarf virus transmission by the aphid Rhopalosiphum padi

2,4-Dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA), a hydroxamic acid (Hx) occurring in wheat, was shown to deter feeding by the aphid Rhopalosiphum padi (L.), and to reduce BYDV transmission to the plant. Dual choice tests with wheat leaves showed the preferential settlement of aphids on leaves with lower levels of DIMBOA. Electric monitoring of aphid feeding behaviour showed that in seedlings with higher DIMBOA levels fewer aphids reached the phloem and they needed longer times to contact a phloem vessel than in those with lower levels. When aphids carrying BYDV were allowed to feed on wheat cultivars with different DIMBOA levels, fewer plants were infected with BYDV in the higher DIMBOA cultivars than in the lower ones. Preliminary field experiments showed a tendency for wheat cultivars with higher Hx levels to be more tolerant to infection by BYDV than lower Hx level ones.     

Interactions of Russian wheat aphid, a hymenopterous parasitoid and resistant and susceptible slender wheatgrasses

Interactions among three trophic levels of resistant and susceptible slenderwheat grasses, Elymus trachycaulum (Link) Goule ex Shinners ex. H.F. Lewis, Russian wheat aphid, Diuraphis noxia (Mordvilko), and a hymenopterous parasitoid were studied in the laboratory and greenhouse. These relationships were compared with a commercial susceptible wheat Triticum aestivum L. variety. Aphids reared on the resistant entries showed significantly lower weights and numbers. Significant reduction of parasitoid mummy weight and adult size was positively correlated with the effects on the aphids. Resistant entries also induced a longer prereproductive period for both the aphids and parasitoids. Numbers of aphids and aphid damage were significantly modified by the addition of parasitoids. Parasitism was higher on plants that did not have leaf rolling. These findings may indicate that antibiosis resistance studied here is not the most desirable because it decreases natural enemy vitality.     

Abundance and natural control of the woolly aphid <Emphasis Type="Italic">Eriosoma lanigerum</Emphasis> in an Australian apple orchard IPM program

Woolly aphid (Eriosoma lanigerum Hausmann) (Hemiptera: Aphididae), was monitored over three growing seasons (1995--1998) to assess its abundance and management under apple IPM programs at Bathurst on the Central Tablelands of NSW, Australia. Woolly aphid infestations were found to be extremely low in IPM programs utilising mating disruption and fenoxycarb for codling moth Cydia pomonella L. (Lepidoptera: Tortricidae) control. This was the direct result of increased numbers of natural enemies. No insecticides were applied for woolly aphid control. Under the IPM strategies tested the principal control agent was identified as European earwig (Forficula auricularia L.) (Dermaptera: Forficulidae). Earwigs in combination with Aphelinus mali (Haldeman) (Hymenoptera: Aphelinidae) reduced woolly aphid infestations below the action threshold set by commercial growers. However, A. mali together with other flying natural enemies, e.g., ladybirds, lacewings and hoverflies, did not provide commercially acceptable control of woolly aphid in the absence of earwigs. Under the conventional spray program, using the broad-spectrum insecticide azinphos-methyl for codling moth control, the level of woolly aphid infestation increased with each successive season and biological control was not established. When azinphos-methyl was withdrawn, natural enemies migrated in and provided control of woolly aphid within one season. This is the first study to show that the biological control of woolly aphid can be achieved in a commercially viable IPM program.     

Comparative population structure of Chinese sumac aphid <Emphasis Type="Italic">Schlechtendalia chinensis</Emphasis> and its primary host-plant <Emphasis Type="Italic">Rhus chinensis</Emphasis>

Most of our current understanding of comparative population structure has been come from studies of parasite–host systems, whereas the genetic comparison of gallnut-aphids and their host-plants remain poorly documented. Here, we examined the population genetic structure of the Chinese sumac aphid Schlechtendalia chinensis and its unique primary host-plant Rhus chinensis in a mountainous province in western China using inter-simple sequence repeat (ISSR) markers. Despite being sampled from a mountainous geographic range, analysis of molecular variance (AMOVA) showed that the majority of genetic variation occurred among individuals within populations of both the aphid and its host. The aphid populations were found to be structured similarly to their primary host populations (F _ST values were 0.239 for the aphid and 0.209 for its host), suggesting that there are similar patterns of gene flow between the populations of the aphid and between populations of its host-plant. The genetic distances (F _ST/1 − F _ST) between the aphid populations and between its host-plant populations were uncorrelated, indicating that sites with genetically similar host-plant populations may not always have genetically similar aphid populations. The lack of relationships between genetic and geographical distance matrices suggested that isolation by distance (IBD) played a negligible role at this level. This may be mainly attributed to the founder effect, genetic drift and the relative small spatial scale between populations. Zhumei Ren and Bin Zhu contributed equally to this work.     

Induction of sexual forms in the rose aphid Macrosiphum rosae

The rose aphid, Macrosiphum rosae (L.), was tested for its ability to produce sexual forms on rose leaves, after induction by environmental conditions in the field and in the laboratory. Clones were collected in Tübingen, Federal Republic of Germany, and in south-eastern New South Wales, Australia. The German clones all produced sexual forms, while the response of the Australian clones was weak. There appeared to be a bias in the sex ratio towards females: This is discussed in developmental terms. The environmental and genetic factors influencing the response are considered.     

Low field performance of an aphid parasitoid,Aphelinus abdominalis,efficient in the laboratory [Hym., Aphelinidae]

Life history traits of two inbred lines of the aphid parasitoidAphelinus abdominalis (Dalman) were evaluated in the laboratory. Both lines exhibited high fecundities, produced a high proportion of female offspring and showed to be long-lived. However, release experiments in winter wheat fields failed to achieve establishment of the parasitoids. In addition, the wasps parasitized considerably fewer aphids in two types of field cages than they did in the laboratory. AsA. abdominalis eggs and/or larvae arrested in development were not found in dissected aphids from field cages, we conclude that the wasps were unable or unwilling to parasitize high numbers of hosts in the cages. The reason for this odd behaviour is unknown.     

Ladybird population dynamics in potato: comparison of native species with an invasive species, Harmonia axyridis

Following the detection of the harlequin ladybird, Harmonia axyridis, in 2003 in potato crops in Belgium, a study was carried out between 2004 and 2006 on the phenology of this species compared to native species in potato. The results confirmed the success of H. axyridis, with high population levels in 2004 and 2005. In 2006, aphid populations were very low and no H. axyridis larvae were sampled in potato, but the indigenous species Coccinella septempunctata and Propylea quatuordecimpunctata were detected. A species by species comparison of the date of first larvae detection, the larvae population peak, and the difference between this peak and the aphid population peak was performed. Results showed a clear correlation between C. septempunctata and P. quatuordecimpunctata and potato aphids, with a delay of 3.5 and 6.5 days between the aphid and ladybird population peaks for the two native species. H. axyridis arrived 7–8 days after the two indigenous species and the larval peak population occurred 15.8 days after the aphid population peak. This meant that H. axyridis had to complete its larval development with very low aphid populations or even with no aphids at all. The reason for its late arrival and the possible food resources used by H. axyridis larvae are discussed.     

Host-specificity and virus-vector potential ofAphis chloris [Hemiptera: Aphididae], a biological control agent for St John's wort in Australia

Under laboratory conditionsAphis chloris Koch has been demonstrated to be specific to plants belonging to the genusHypericum. It can effect severe damage to its principal host,H. perforatum L., and shows good potential for contributing to the control of this noxious weed. Other species ofHypericum are less favoured hosts ofA. chloris and would not be endangered by it. A. chloris shows a high level of host-discrimination and does not transmit persistent viruses between non-host plants. Whereas in the laboratory it is capable of transmitting non-persistent viruses, it would contribute only marginally to the risk of virus transfer posed by the Australian aphid fauna as a whole, and its release would not necessitate changes to existing control practices, where these are required to reduce plant virus transmission. As a consequence,A. chloris is considered safe for release againstH. perforatum in Australia.      

Wheat containing snowdrop lectin (GNA) does not affect infection of the cereal aphid <Emphasis Type="Italic">Metopolophium</Emphasis><Emphasis Type="Italic">dirhodum</Emphasis> by the fungal natural enemy<Emphasis Type="Italic">Pandora neoaphidis</Emphasis>

Studies were carried out to determine if susceptibility of the cereal aphid Metopolophium dirhodum to the fungus Pandora neoaphidis was affected by wheat expressing snowdrop lectin (GNA). Aphid infection did not differ significantly between the transgenic GNA and non-transformed lines (91 and 82%, respectively). Fecundity also did not differ between aphids on the two lines, and was ca. 18 nymphs adult⁻¹. Time to infection was ca. 5 days for M. dirhodum on both lines in two of three assays. Our results indicate that wheat expressing GNA would not compromise the efficacy of P. neoaphidis as a biocontrol agent.     

Hyperpredation by generalist predatory mites disrupts biological control of aphids by the aphidophagous gall midge Aphidoletes aphidimyza

Biological control of different species of pest with various species of generalist predators can potentially disrupt the control of pests through predator-predator interactions. We evaluate the impact of three species of generalist predatory mites on the biological control of green peach aphids, Myzus persicae (Sulzer) with the aphidophagous gall midge Aphidoletes aphidimyza (Rondani). The predatory mites tested were Neoseiulus cucumeris (Oudemans), Iphiseius degenerans (Berlese) and Amblyseius swirskii Athias–Henriot, which are all commonly used for pest control in greenhouse sweet pepper. All three species of predatory mites were found to feed on eggs of A. aphidimyza, even in the presence of abundant sweet pepper pollen, an alternative food source for the predatory mites. In a greenhouse experiment on sweet pepper, all three predators significantly reduced population densities of A. aphidimyza, but aphid densities only increased significantly in the presence of A. swirskii when compared to the treatment with A. aphidimyza only. This stronger effect of A. swirskii can be explained by the higher population densities that this predator reached on sweet pepper plants compared to the other two predator species. An additional experiment showed that female predatory midges do not avoid oviposition sites with the predator A. swirskii. On the contrary, they even deposited more eggs on plants with predatory mites than on plants without. Hence, this study shows that disruption of aphid control by predatory mites is a realistic scenario in sweet pepper, and needs to be considered when optimizing biological control strategies.     

A possibly new Rickettsia-like genus symbiont is found in Chinese wheat pest aphid, Sitobion miscanthi (Hemiptera: Aphididae)

In this study, we investigated Rickettsia infection in Chinese wheat pest aphid (Sitobion miscanthi), moreover detected a possibly new Rickettsia-like symbiont, provisionally named as SMLS¹ (S. miscanthi L type symbiont). The sequence of SMLS 16S rRNA gene is 94% similar to that of its presumed closest relative, Orientiatsutsugamushi. If levels of divergence indicate taxonomic distinctiveness, SMLS probably represents a new genus in the family Rickettsiaceae. SMLS occurs in most populations of S. miscanthi, and with divergent infection frequencies, from 5.0% to 93.8%.     

Genetic variation in the effect of a facultative symbiont on host-plant use by pea aphids

Ecological specialisation on different host plants occurs frequently among phytophagous insects and is normally assumed to have a genetic basis. However, insects often carry microbial symbionts, which may play a role in the evolution of specialisation. The bacterium Regiella insecticola is a facultative symbiont of pea aphids (Acyrthosiphon pisum) where it is found most frequently in aphid clones feeding on Trifolium giving rise to the hypothesis that it may improve aphid performance on this plant. A study in which R. insecticola was eliminated from a single naturally infected aphid clone supported the hypothesis, but a second involving two aphid clones did not find the same effect. We created a series of new pea aphid–R. insecticola associations by injecting different strains of bacteria into five aphid clones uninfected by symbionts. For all aphid clones, the bacteria decreased the rate at which aphids accepted Vicia faba as a food plant and reduced performance on this plant. Their effect on aphids given Trifolium pratense was more complex: R. insecticola negatively affected acceptance by all aphid clones, had no effect on the performance of four aphid clones, but increased performance of a fifth, thus demonstrating genetic variation in the effect of R. insecticola on pea aphid host use. We discuss how these results may explain the distribution and frequency of this symbiont across different aphid populations. Julia Ferrari and Claire L. Scarborough contributed equally to the work.     

Indirect Effect of a Transgenic Wheat on Aphids through Enhanced Powdery Mildew Resistance

In agricultural ecosystems, arthropod herbivores and fungal pathogens are likely to colonise the same plant and may therefore affect each other directly or indirectly. The fungus that causes powdery mildew (Blumeria graminis tritici) and cereal aphids are important pests of wheat but interactions between them have seldom been investigated. We studied the effects of powdery mildew of wheat on two cereal aphid species, Metopolophium dirhodum and Rhopalosiphum padi. We hypothesized that aphid number and size will be smaller on powdery mildew-infected plants than on non-infected plants. In a first experiment we used six commercially available wheat varieties whereas in the second experiment we used a genetically modified (GM) mildew-resistant wheat line and its non-transgenic sister line. Because the two lines differed only in the presence of the transgene and in powdery mildew resistance, experiment 2 avoided the confounding effect of variety. In both experiments, the number of M. dirhodum but not of R. padi was reduced by powdery mildew infection. Transgenic mildew-resistant lines therefore harboured bigger aphid populations than the non-transgenic lines. For both aphid species individual size was mostly influenced by aphid number. Our results indicate that plants that are protected from a particular pest (powdery mildew) became more favourable for another pest (aphids).     

The mitochondrial genome of the Russian wheat aphid Diuraphis noxia: Large repetitive sequences between trnE and trnF in aphids

To characterize aphid mitochondrial genome (mitogenome) features, we sequenced the complete mitogenome of the Russian wheat aphid, Diuraphis noxia. The 15,784-bp mitogenome with a high A + T content (84.76%) and strong C skew (− 0.26) was arranged in the same gene order as that of the ancestral insect. Unlike typical insect mitogenomes, D. noxia possessed a large tandem repeat region (644 bp) located between trnE and trnF. Sequencing partial mitogenome of the cotton aphid (Aphis gossypii) further confirmed the presence of the large repeat region in aphids, but with different repeat length and copy number. Another motif (58 bp) tandemly repeated 2.3 times in the control region of D. noxia. All repeat units in D. noxia could be folded into stem-loop secondary structures, which could further promote an increase in copy numbers. Characterization of the D. noxia mitogenome revealed distinct mitogenome architectures, thus advancing our understanding of insect mitogenomic diversities and evolution.     

In vitro enzymatic chlorophyll catabolism in wheat elicited by cereal aphid feeding

Chlorophyll degradation is a complex phenomenon that often accompanies insect feeding damage to plants. Loss of chlorophyll can be initiated by several reactions, including oxidative bleaching, chlorophyllase activity, and Mg-dechelatase activity. Extracts from the Russian wheat aphid [Diuraphis noxia (Mordvilko)], the bird cherry-oat aphid [Rhopalosiphum padi (L.)], and aphid-infested and uninfested wheat plants were assayed in vitro for activities involved in chlorophyll degradation. Although the initial infestation was the same (10 apterous adults) for both aphid species, D. noxia weight was significantly higher than R. padi after feeding for 12 days. Consequently, D. noxia feeding caused greater fresh leaf weight reduction than R. padi feeding. Chlorophyll degradation assays showed no activity from either D. noxia or R. padi extracts. Plant extract assays showed a significant difference in Mg-dechelatase activity, while no difference was detected in either the chlorophyllase or oxidative bleaching pathways among the aphid-infested or uninfested plant extracts. Diuraphis noxia-infested leaf extracts showed a greater increase of Mg-dechelatase activity than either R. padi-infested or the uninfested plants. The findings suggest that leaf chlorosis elicited by D. noxia feeding is different from the chlorophyll degradation that occurs in natural plant senescence. Aphid-elicited chlorosis might be the result of a Mg-dechelatase-driven catabolism of chlorophyll in challenged wheat seedlings, however, the factor(s) from D. noxia that elicited the increase of Mg-dechelatase activity still remain to be determined.     

Release and recovery in South Africa of the exotic aphid parasitoid <Emphasis Type="Italic">Aphelinus hordei</Emphasis> verified by the polymerase chain reaction

The exotic aphid parasitoid Aphelinushordei Kurdjumov (Hymenoptera: Aphelinidae) was released at five Russian wheat aphid [Diuraphis noxia (Mordvilko)] infested wheat fields in the eastern parts of the Free State Province of South Africa during the 1998 and 1999 growing seasons. Except for differences in the setae on the ventralside of the forewings, this species is verysimilar in colour and structure to A.varipes (Foerster) and A. albipodusHayat & Fatima, which also parasitise D.noxia. It is therefore difficult todistinguish between them, and to determinetheir establishment. Therefore a polymerasechain reaction, using specific primers for bothITS2 and mitochondrial 16s DNA sequencesof the three parasitoids, followed by HinfIrestriction endonuclease digestion and agarosegel electrophoresis, was tested to distinguishbetween them. Parasitoid recoveries were madeat the release sites within weeks after theywere released. Putative individuals of A.hordei were also collected during 1999 and2000 on D. noxia in Lesotho, whichis situated on the eastern border of the FreeState Province. The procedure separated the three Aphelinus spp.reliably. Between 94 and 100% of theindividuals recovered during the two fieldseasons were identified as being A.hordei, thus verifying recovery of this exoticaphid parasitoid in South Africa.