Parasitism of soybean aphid by Aphelinus species on soybean susceptible versus resistant to the aphid

The soybean aphid, Aphis glycines, is native to Asia, but during the last decade it has invaded North America, where it has spread to most soybean growing regions and become the most important insect pest of soybean. Current control of soybean aphid relies primarily on insecticides, but alternatives to insecticidal control are being explored, especially host plant resistance and biological control, which may interact positively or negatively. Research on host plant resistance to the soybean aphid has revealed six genes that affect resistance. We measured the impact of the two most studied resistance loci, Rag1 and Rag2, on two parasitoid species: Aphelinus glycinis, a recently described species from Asia, which is being introduced into the USA to control the soybean aphid, and Aphelinus certus, also from Asia but accidentally introduced into the USA. Resistance did not affect oviposition by either parasitoid species. However, resistance did reduce successful parasitism by A. glycinis, with each resistance allele causing a two-fold reduction in number of mummified aphids. The resistance alleles did not affect adult emergence, sex ratio, or the size of A. glycinis. For A. certus, the Rag1 resistance allele had no effect on parasitism, while the Rag2 resistance allele reduced parasitism four-fold. On the other hand, the Rag1 resistance allele increased the frequency of males among progeny and decreased female size of A. certus. Despite the reduction in parasitism, these parasitoids are nonetheless able to parasitize the soybean aphid on resistant soybean, which means that they should still contribute to the management of soybean aphid on resistant varieties.     

Field and laboratory evaluations of soybean lines against soybean aphid (Hemiptera: Aphididae)

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is a major pest of soybean, Glycine max (L.). Merr., that significantly reduces yield in northern production areas of North America. Insecticides are widely used to control soybean aphid outbreaks, but efforts are underway to develop host plant resistance as an effective alternative management strategy. Here, previously identified resistant lines were evaluated in laboratory tests against field-collected populations of soybean aphid and in field-plot tests over 2 yr in South Dakota. Six lines previously identified with resistance to soybean aphid--Jackson, Dowling, K1639, Cobb, Palmetto and Sennari--were resistant in this study, but relatively high aphid counts on Tie-feng 8 in field plots contrasted with its previously reported resistance. Bhart-PI 165989 showed resistance in one of two laboratory tests, but it had relatively large aphid infestations in both years of field tests. Intermediate levels of soybean aphid occurred in field plots on lines previously shown to have strong (Sugao Zairai, PI 230977, and D75-10169) or moderate resistance to soybean aphid (G93-9223, Bragg, Braxton, and Tracy-M). Sugao Zairai also failed to have a significant proportion of resistant plants in two laboratory tests against aphids field-collected in 2008, but it was resistant in laboratory tests with aphids collected in 2002, 2005, and 2006. Overall, results showed that lines with Rag (i.e., Jackson) or Rag1 gene (i.e., Dowling) had low aphid numbers, whereas lines with Rag2 (i.e., Sugao Zairai, Sennari) had mixed results. Collectively, responses of soybean aphid populations in laboratory and field tests in 2008 resembled a virulence pattern reported previously for biotype 3 soybean aphids, but virulence in soybean aphid populations was variable and dynamic over years of the study. These results, coupled with previous reports of biotypes virulent to Rag1, suggest that deployment of lines with a single aphid-resistance gene is limited for soybean aphid management, and that deployment strategies relying on multiple resistance genes may be needed to effectively use plant resistance against soybean aphid.     

Effects of plant protease inhibitors, oryzacystatin I and soybean Bowman-Birk inhibitor, on the aphid Macrosiphum euphorbiae (Homoptera, Aphididae) and its parasitoid Aphelinus abdominalis (Hymenoptera, Aphelinidae)

Transgenic plants expressing protease inhibitors (PIs) have emerged in recent years as an alternative strategy for pest control. Beneficial insects such as parasitoids may therefore be exposed to these entomotoxins either via the host or by direct exposure to the plant itself. With the objective of assessing the effects of PIs towards aphid parasitoids, bioassays using soybean Bowman-Birk inhibitor (SbBBI) or oryzacystatin I (OCI) on artificial diet were performed on Macrosiphum euphorbiae-Aphelinus abdominalis system. OCI significantly reduced nymphal survival of the potato aphid M. euphorbiae and prevented aphids from reproducing. This negative effect was much more pronounced than with other aphid species. On the contrary, SbBBI did not affect nymphal viability but significantly altered adult demographic parameters. Enzymatic inhibition assays showed that digestive proteolytic activity of larvae and adults of Aphelinus abdominalis predominantly relies on serine proteases and especially on chymotrypsin-like activity. Immunoassays suggested that OCI bound to aphid proteins and accumulated in aphid tissues, whereas SbBBI remained unbound in the gut. Bioassays using M. euphorbiae reared on artificial diets supplemented with both OCI and SbBBI showed a fitness impairment of Aphelinus abdominalis that developed on intoxicated aphids. However, only SbBBI was detected in parasitoid larvae, while no PI could be detected in adult parasitoids that emerged from PI-intoxicated aphids. The potential impact of PI-expressing plants on aphid parasitoids and their combined efficiency for aphid control are discussed.     

Combined effects of host-plant resistance and intraguild predation on the soybean aphid parasitoid Binodoxys communis in the field

Soybean varieties that exhibit resistance to the soybean aphid Aphis glycines have been developed for use in North America. In principle, host-plant resistance to soybean aphid can influence the interactions between the soybean aphid and its natural enemies. Resistance could change the quality of soybean aphids as a food source, the availability of soybean aphids, or resistance traits could directly affect aphid predators and parasitoids. Here, we focus on the effect of soybean aphid resistance on the interactions between soybean aphids, the parasitoid Binodoxys communis (Hymenoptera: Braconidae), and predators of these two species. We determined whether host-plant resistance affected within-season persistence of B. communis by releasing parasitoids into resistant and susceptible soybean plots. We observed higher B. communis densities in susceptible soybean plots than in resistant plots. There were also higher overall levels of intraguild predation of B. communis in susceptible plots, although the per-capita risk of intraguild predation of B. communis was affected neither by plant genotype nor by aphid density. We discuss these effects and whether they were caused by direct effects of the resistant plants on B. communis or indirect effects through soybean aphid or predators.     

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.     

Compatibility of aphid resistance in soybean and biological control by the parasitoid Aphidius colemani (Hymenoptera: Braconidae)

Biological control and soybean cultivars bred for increased resistance to the soybean aphid (Aphis glycines) are two approaches used to manage this serious pest of soybeans in North America. However, as with many other pest systems, the compatibility of these two pest management approaches has not been studied in detail. The aphidiine wasp Aphidius colemani is one of several candidate species for biological control of the soybean aphid in soybean in North America. Resistance to the soybean aphid in the USDA soybean cultivar Dowling is largely controlled by a single dominant gene Rag1, which is the focus of plant breeding programs directed against the soybean aphid. In this study, we measured developmental and behavioral differences in the parasitic wasp A. colemani when it attacked soybean aphids feeding on either the aphid-resistant Dowling or aphid-susceptible Glenwood cultivars of soybean. We used a combination of choice and no-choice experiments to examine the effects of host plant cultivar on the number of parasitized aphids formed and the sex ratio and body weights of adult offspring produced. Significantly more aphids were parasitized when they fed on Glenwood compared to Dowling and these offspring were larger when they developed in aphids that fed on Glenwood soybeans. To distinguish between effects on foraging decisions and offspring survivorship, we conducted an additional experiment that followed the oviposition decisions and fate of each parasitized aphid. Foraging female A. colemani spent less time handling individual aphids and encountered and attacked aphids at a higher rate when they fed on aphids feeding on Glenwood soybeans than aphids feeding on Dowling soybeans. Furthermore, wasp survivorship in aphids was greater on Glenwood than Dowling. Taken together, aphid-resistance in soybeans has negative effects on foraging behavior and offspring fitness of A. colemani raising concerns about the compatibility of these two pest management approaches.     

Performance and prospects of Rag genes for management of soybean aphid

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is an invasive insect pest of soybean [Glycine max (L.) Merr. (Fabaceae)] in North America, and it has led to extensive insecticide use in northern soybean‐growing regions there. Host plant resistance is one potential alternative strategy for managing soybean aphid. Several Rag genes that show antibiosis and antixenosis to soybean aphid have been recently identified in soybean, and field‐testing and commercial release of resistant soybean lines have followed. In this article, we review results of field tests with soybean lines containing Rag genes in North America, then present results from a coordinated regional test across several field sites in the north‐central USA, and finally discuss prospects for use of Rag genes to manage soybean aphids. Field tests conducted independently at multiple sites showed that soybean aphid populations peaked in late summer on lines with Rag1 or Rag2 and reached economically injurious levels on susceptible lines, whereas lines with a pyramid of Rag1 + Rag2 held soybean aphid populations below economic levels. In the regional test, aphid populations were generally suppressed by lines containing one of the Rag genes. Aphids reached putative economic levels on Rag1 lines for some site years, but yield loss was moderated, indicating that Rag1 may confer tolerance to soybean aphid in addition to antibiosis and antixenosis. Moreover, no yield penalty has been found for lines with Rag1, Rag2, or pyramids. Results suggest that use of aphid‐resistant soybean lines with Rag genes may be viable for managing soybean aphids. However, virulent biotypes of soybean aphid were identified before release of aphid‐resistant soybean, and thus a strategy for optimal deployment of aphid‐resistant soybean is needed to ensure sustainability of this technology.     

Seasonal abundance of resident parasitoids and predatory flies and corresponding soybean aphid densities, with comments on classical biological control of soybean aphid in the Midwest

Seasonal abundance of resident parasitoids and predatory flies, and corresponding soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), densities were assessed in soybean fields from 2003 to 2006 at two locations in lower Michigan. Six parasitoid and nine predatory fly species were detected in 4 yr by using potted plants infested with soybean aphid placed in soybean fields. The parasitoid Lysiphlebus testaceipes Cresson (Hymenoptera: Braconidae) and the predatory flies Aphidoletes aphidimyza Rondani (Diptera: Cecidomyiidae), and Allograpta obliqua Say (Diptera: Syrphidae) were most numerous. Generally, L. testaceipes was more abundant late in the soybean growing season, but it also occurred during soybean vegetative growth; A. obliqua was more abundant during vegetative growth; and A. aphidimyza was common throughout the season. Soybean plants were visually inspected to estimate densities of soybean aphid, mummified aphids, and immature predatory flies. From 2003 to 2006, parasitism rates were inversely correlated with aphid density: percentage of parasitism was always very low (< or = 0.1%) at high aphid densities (> 100 aphids per plant), and higher parasitism, up to 17%, was observed at very low aphid densities (< 1 aphid per plant). Populations of immature predatory flies, particularly A. aphidimyza, generally increased in soybean fields with increasing soybean aphid populations, but aphids always outnumbered immature flies by 100-21,000-fold when flies were detected. Rearing field-collected aphid in 2006 substantiated that parasitism varied widely, with parasitism in most cases < 10%. Based on findings of low parasitism and predation, positive response to changing aphid densities by predatory flies but not parasitoids, early season abundance primarily of predatory flies, and past findings on these taxa's diversity and abundance, we discuss the potential use of exotic parasitoids and predatory flies to enhance soybean aphid biological control.     

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.     

Potential effects of plant protease inhibitors, oryzacystatin I and soybean Bowman-Birk inhibitor, on the aphid parasitoid Aphidius ervi Haliday (Hymenoptera, Braconidae)

Protease inhibitors (PIs) have been shown to cause lethal and sublethal effects on aphids depending on the kind of PI and aphid species. Therefore, these proteins might affect aphid parasitoids directly by inhibiting their digestive proteolysis or indirectly via their development in a less suitable host. In our study, the risk of exposure and the potential effects of soybean Bowman-Birk inhibitor (SbBBI) and oryzacystatin I (OCI) on the aphid endoparasitoid Aphidius ervi were investigated using artificial diet to deliver PIs. Immunoassays showed that both SbBBI and OCI were detected in the honeydew of aphids reared on artificial diet containing these recombinant proteins at 100 microg/mL. However, only SbBBI was detected in parasitoid larvae, while this PI could not be detected in adult parasitoids emerged from PI-intoxicated aphids. Enzymatic inhibition assays showed that digestive proteolytic activity of larvae and adults of A. ervi predominantly relies on serine proteases and especially on chymotrypsin-like activity. Bioassays using SbBBI and OCI on artificial diet were performed. A. ervi that developed on intoxicated aphids had impaired fitness. Thus development and parasitism success of parasitoids exposed to OCI were severely affected. On the contrary, SbBBI only altered significantly female size and sex ratio. Direct exposure to PIs through adult food intake did not affect female's longevity, while SbBBI and OCI (100 microg/mL) induced 69% and 30% inhibition of digestive protease activity, respectively. These studies made it possible to estimate the risk of exposure to plant PIs and the sensitivity of the aphid parasitoid A. ervi to these entomotoxins, by combining immunological, biochemical and biological approaches. First it pointed out that only immature stages are affected by PIs. Secondly, it documented two different modes of effect, according to the nature of the PIs and both host and parasitoid susceptibility. OCI prevented the development of A. ervi mainly due to the host susceptibility, whereas SbBBI only induced sublethal effects on the parasitoid, possibly due to both direct action on the parasitoid susceptible proteases, and host-mediated action through size reduction.     

Parasitism of the soybean aphid, Aphis glycines by Binodoxys communis: the role of aphid defensive behaviour and parasitoid reproductive performance

The Asian parasitoid, Binodoxys communis (Gahan) (Hymenoptera: Braconidae), is a candidate for release against the exotic soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), in North America. In this study, we examined preferences by B. communis for the different developmental stages of A. glycines and investigated consequences of these preferences for parasitoid fitness. We also determined to what extent aphid defensive behaviours mediate such preferences. We found that B. communis readily attacks and successfully develops in the different A. glycines developmental stages. Binodoxys communis development time gradually increased with aphid developmental stage, and wasps took longest to develop in alates. An average (+/-SE) of 54.01+/-0.08% of parasitized A. glycines alatoid nymphs transformed into winged adult aphids prior to mummification. No-choice assays showed a higher proportion of successful attacks for immature apterous A. glycines nymphs compared to adults and alatoid nymphs. Also, choice trials indicated avoidance and lower attack and oviposition of adults and alatoid nymphs. The different aphid stages exhibited a range of defensive behaviours, including body raising, kicking and body rotation. These defenses were employed most effectively by larger aphids. We discuss implications for the potential establishment, spread and biological control efficacy of A. glycines by B. communis in the event that it is released in North America.     

Impacts of thiamethoxam seed treatment and host plant resistance on the soybean aphid fungal pathogen, Pandora neoaphidis

Since the introduction of soybean aphid, Aphis glycines Matsumura, from Asia, insecticide use in soybean has increased substantially in the north central United States. Insecticide seed treatments and aphid resistant soybean varieties are management tactics that may reduce reliance on foliar applications of broad-spectrum insecticides. Exploring potential nontarget impacts of these technologies will be an important step in incorporating them into aphid management programs. We investigated impacts of thiamethoxam seed treatment and Rag1 aphid resistant soybean on a fungal pathogen of soybean aphid, Pandora neoaphidis (Remaudière & Hennebert) Humber, via open plot and cage studies. We found that although thiamethoxam seed treatment did significantly lower aphid pressure in open plots compared with an untreated control, this reduction in aphid density translated into nonsignificant decreases in fungal disease prevalence in aphids. Furthermore, when aphid densities were approximately equal in seed treated and untreated soybean, no impact on aphid fungal disease was observed. In open plots, Rag1 resistant soybean experienced lower aphid pressure and aphid disease prevalence compared with a nonresistant isoline. However, in cages when aphid densities were equivalent in both resistant and susceptible soybean, resistance had no impact on aphid disease prevalence. The addition of thiamethoxam seed treatment to resistant soybean yielded aphid densities and aphid disease prevalence similar to untreated, resistant soybean. These studies provide evidence that thiamethoxam seed treatments and Rag1 resistance can impact P. neoaphidis via decreased aphid densities; however, this impact is minimal, implying use of seed treatments and host plant resistance are compatible with P. neoaphidis.     

Effects of Rag1 aphid‐resistant soybean on mortality,development, and preference of brown marmorated stink bug

The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), poses a new threat to soybean, Glycine max (L.) Merrill (Fabaceae), production in the north central USA. As H. halys continues to spread and increase in abundance in the region, the interaction between H. halys and management tactics deployed for other pests must be determined. Currently, the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is the most abundant and damaging insect pest of soybean in the region. Aphid‐resistant soybean, mainly with the Rag1 gene, is commercially available for management of A. glycines. Here, experiments were performed to evaluate the effects of Rag1 aphid‐resistant soybean on the mortality, development, and preference of H. halys. In a no‐choice test, mortality of H. halys reared on Rag1 aphid‐resistant soybean pods was significantly lower than when reared on aphid‐susceptible soybean pods (28 vs. 53%). Development time, adult weight, and proportion females of surviving adults did not differ when reared on Rag1 aphid‐resistant or aphid‐susceptible soybean pods. In choice tests, H. halys exhibited a preference for Rag1 aphid‐resistant over aphid‐susceptible soybean pods after 4 h, but not after 24 h. Halyomorpha halys exhibited no preference when tested with vegetative‐stage or reproductive‐stage soybean plants. The preference by H. halys for Rag1 aphid‐resistant soybean pods and the decreased mortality when reared on these pods suggests that the use of Rag1 aphid‐resistant soybean may favor this emerging pest in the north central USA.     

Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study

In order to reduce parasite‐induced mortality, hosts may be involved in mutualistic interactions in which the partner contributes to resistance against the parasite. The pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae), harbours secondary bacterial endosymbionts, some of which have been reported to confer resistance against aphid parasitoids. Although this resistance often results in death of the developing parasitoid larvae, some parasitoid individuals succeed in developing into adults. Whether these individuals suffer from fitness reduction compared to parasitoids developing in pea aphid clones without symbionts has not been tested so far. Using 30 pea aphid clones that differed in their endosymbiont complement, we studied the effects of these endosymbionts on aphid resistance against the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae), host–parasitoid physiological interactions, and fitness of emerging adult parasitoids. The number of symbiont species in an aphid clone was positively correlated with a number of resistance measurements but there were also clear symbiont‐specific effects on the host–parasitoid interaction. As in previous studies, pea aphid clones infected with Hamiltonella defensa Moran et al. showed resistance against the parasitoid. In addition, pea aphid clones infected with Regiella insecticola Moran et al. and co‐infections of H. defensa–Spiroplasma, R. insecticola–Spiroplasma, and R. insecticola–H. defensa showed reduced levels of parasitism and mummification. Parasitoids emerging from symbiont‐infected aphid clones often had a longer developmental time and reduced mass. The number of teratocytes was generally lower when parasitoids oviposited in aphid clones with a symbiont complement. Interestingly, unparasitized aphids infected with Serratia symbiotica Moran et al. and R. insecticola had a higher fecundity than unparasitized aphids of uninfected pea aphid clones. We conclude that in addition to conferring resistance, pea aphid symbionts also negatively affect parasitoids that successfully hatch from aphid mummies. Because of the link between aphid resistance and the number of teratocytes, the mechanism underlying resistance by symbiont infection may involve interference with teratocyte development.     

Antagonistic effects of soybean viruses on soybean aphid performance

Although there is long-standing recognition that pest complexes require different management approaches than individual pests, relatively little research has explored how pests interact. In particular, little is known of how herbivorous insects and plant pathogens interact when sharing the same host plant. The soybean aphid, Aphis glycines Mastumura, a recently introduced pest of soybean in the upper midwestern United States, and a complex of plant viruses vectored to soybean by insects have become a major concern for growers in the region. Given the abundance of soybean aphid and the increase in virus incidence in recent years, soybean aphids often use soybean infected by plant viral pathogens. We tested the hypothesis that soybean aphid performance is affected by virus infection of soybean plants. We conducted a series of field and laboratory experiments that examined how infection of soybeans with the common plant viruses, alfalfa mosaic, soybean mosaic, and bean pod mottle viruses, influenced soybean aphid performance. Soybean plants (in the field and laboratory) were hand inoculated with individual viruses, and aphids were allowed to colonize plants naturally in field experiments or added to the plants in clip-cages or within mesh bags in laboratory assays. In the field, aphid density on uninfected control soybean plants was nearly double that on infected plants. In laboratory assays, aphid population growth rates were on average 20% lower for aphids on virus infected compared with uninfected plants. Life table analyses showed that increased mortality on virus-infected plants likely explain differences in aphid population growth. Although there was some heterogeneity in the significance of treatment effects among different experiments, when independent experiments are taken together, there is on average an overall negative effect of these viruses on soybean aphids.     

Genetic linkage mapping of the soybean aphid resistance gene in PI 243540

The soybean aphid (Aphis glycines Matsumura) is a pest of soybean [Glycine max (L.) Merr.] in many soybean growing countries of the world, mainly in Asia and North America. A single dominant gene in PI 243540 confers resistance to the soybean aphid. The objectives of this study were to identify simple sequence repeat (SSR) markers closely linked to the gene in PI 243540 and to position the gene on the consensus soybean genetic map. One hundred eighty-four F(2) plants and their F(2:3) families from a cross between the susceptible cultivar Wyandot and PI 243540, and the two parental lines were screened with the Ohio biotype of soybean aphid using greenhouse choice tests. A SSR marker from each 10-cM section of the consensus soybean map was selected for bulked segregant analysis (BSA) to identify the tentative genomic location of the gene. The BSA technique was useful to localize the gene to a genomic region in soybean linkage group (LG) F. The entire F(2) population was then screened with polymorphic SSR markers from this genomic region and a linkage map with nine SSR markers flanking the gene was constructed. The aphid resistance gene was positioned in the interval between SSR markers Satt334 and Sct_033 on LG F. These SSR markers will be useful for marker assisted selection of this gene. The aphid resistance gene from PI 243540 mapped to a different linkage group than the only named soybean aphid resistance gene, Rag1, from 'Dowling'. Also, the responses of the two known biotypes of the soybean aphid to the gene from PI 243540 and Rag1 were different. Thus, the aphid resistance gene from PI 243540 was determined to be a new and independent gene that has been named Rag2.     

Density-dependent intraguild predation of an aphid parasitoid

A growing body of research has examined the effect of shared resource density on intraguild predation (IGP) over relatively short time frames. Most of this work has led to the conclusion that when the shared resource density is high, the strength of IGP should be lower, due to prey dilution. However, experiments addressing this topic have been done using micro- or mesocosms that excluded the possibility of intraguild predator aggregation. We examined the effect of shared resource density on IGP of an aphid parasitoid in an open field setting where the effects of prey dilution and predator aggregation could occur simultaneously. We brought potted soybean plants with 2, 20, or 200 soybean aphids (Aphis glycines) and 20 pupae (‘mummies’) of the soybean aphid parasitoid Binodoxys communis into soybean fields in Minnesota, USA. We monitored predator aggregation onto the potted plants, predation of parasitoid mummies, and successful adult emergence of B. communis. We found that predator aggregation was higher at the higher aphid densities on our experimental plants and that this coincided with lower adult emergence of B. communis, indicating that even if a prey dilution effect occurred in our study, it was overcome by short-term predator aggregation. Our results suggest that the effect of shared resource density on IGP may be more nuanced in a field setting than in microcosms due to predator aggregation.     

Soybean aphid (Hemiptera: Aphididae) development on soybean with Rag1 alone, Rag2 alone, and both genes combined

Aphis glycines Matsumura (Hemiptera: Aphididae) can reduce the yield of aphid-susceptible soybean (Glycine max (L.) Merrill) cultivars. The Rag1 and Rag2 genes conferresistance to some biotypes of A. glycines. These genes individually can limit population growth of A. glycines and prevent yield loss. The impact of these genes when combined is not known. We compared the development of A. glycines on soybean with Rag1 alone (R1/S2), Rag2 alone (S1/R2), both genes combined (R1/R2), or neither gene (S1/S2). In addition, we determined the impact of different levels of aphid infestation on seed yield. The genotypes were grown in cages and artificially infested with A. glycines to achieve five treatment levels: aphid-free, 675 aphids per plant, 25,000 cumulative aphid days (CAD) (25K), 50,000 CAD (50K), and 75,000 CAD (75K). The S1/S2 line reached the 50K treatment, but did not reach the 75K treatment. Aphid development on R1/S2 and S1/R2 soybeans after two infestations reached a maximum of 25K. The maximum treatment reached on R1/R2 was only 675 aphids per plant after two infestations, at which there was no significant yield reduction when compared with the aphid-free treatment. The maximum yield reduction of S1/S2 was 27% at 50K treatment compared with 2% for R1/S2 and 12% for S1/R2 at the 25K treatment. Our results indicated that for A. glycines used in our study, cultivars with both Rag1 and Rag2 had less aphid exposure and less yield reduction than soybeans with only one resistant gene.     

Soybean aphid intrabiotype variability based on colonization of specific soybean genotypes

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is one of the most destructive insect pests on soybeans in the United States. One method for managing this pest is through host plant resistance. Since its arrival in 2000, 4 aphid biotypes have been identified that are able to overcome soybean aphid resistance (Rag) genes. A soybean aphid isolate collected from Moline, Illinois readily colonized soybean plants with the soybean aphid resistance gene Rag2, unlike biotypes 1 and 2, but similar to soybean aphid biotype 3. Two no‐choice experiments compared the virulence of the Moline isolate with biotype 3. In both experiments, differences in aphid population counts were not significant (P > 0.05) on soybean genotypes LD08–12957a (Rag2) and LD11–5413a (Rag2), but the aphid counts for the Moline isolate were significantly (P < 0.05) lower than the aphid counts for the biotype 3 isolate on the soybean genotypes Dowling (Rag1), LD05–16611 (Rag1), LD11–4576a (Rag1), and PI 567598B (rag1b and rag3). The Moline isolate was a variant of aphid biotype 3, which is the first report showing that soybean aphid isolates classified as the same biotype, based on virulence against specific Rag genes, can differ in aggressiveness or ability to colonize specific host genotypes.     

Effect of three resistant soybean genotypes on the fecundity, mortality, and maturation of soybean aphid (Homoptera: Aphididae)

The fecundity, longevity, mortality, and maturation of the soybean aphid, Aphis glycines Matsumura (Homoptera: Aphididae), were characterized using three resistant soybean, Glycine max (L.) Merrill, genotypes ('Dowling', 'Jackson', and PI200538 'Sugao Zarai') and two susceptible genotypes ('Pana' and 'Loda'). Antibiosis in the resistant genotypes was demonstrated by a significant decrease in fecundity and longevity and increased mortality of A. glycines. Aphid fecundity, measured as number of offspring produced in the first 10 d by each viviparous aptera, was higher on Pana than on the resistant genotypes. Aphid longevity, the mean number of days a 1-d-old adult lived, was 7 d longer on Pana than on Dowling and Jackson. The mortality of both viviparous apterae and nymphs on resistant genotypes was significantly higher than on susceptible genotypes. A greater number of first instars survived to maturation stage (date of first reproduction) on susceptible plants than on resistant plants. None of the first instars placed on Dowling and PI200538 leaves survived to maturation. Observations of aphid behavior on leaves indicated that aphids departed from the leaves of resistant plants 8-24 h after being placed on them, whereas they remained indefinitely on leaves of susceptible cultivars and developed colonies. Reduced feeding due to ingestion of potentially toxic compounds in soybean may explain the possible mechanism of resistance to the soybean aphid.