Deirdre A. Prischmann-Voldseth

Impact of Rag1 Aphid Resistant Soybeans on Binodoxys communis (Hymenoptera: Braconidae), a Parasitoid of Soybean Aphid (Hemiptera: Aphididae)

ABSTRACT Multiple strategies are being developed for pest management of the soybean aphid, Aphis glycines Matsumura; however, there has been little published research thus far to determine how such strategies may influence each other, thereby complicating their potential effectiveness. A susceptible soybean (Glycine max L.) variety without the Rag1 gene and a near isogenic resistant soybean variety with the Rag1 gene were evaluated in the laboratory for their effects on the fitness of the soybean aphid parasitoid, Binodoxys communis (Gahan). The presence or absence of the Rag1 gene was verified by quantifying soybean aphid growth. To test for fitness effects, parasitoids were allowed to attack soybean aphids on either a susceptible or resistant plant for 24 h and then aphids were kept on the same plant throughout parasitoid development. Parasitoid fitness was measured by mummy and adult parasitoid production, adult parasitoid emergence, development time, and adult size. Parasitoids that attacked soybean aphids on susceptible plants produced more mummies, more adult parasitoids, and had a higher emergence rate compared with those on resistant plants. Adult parasitoids that emerged from resistant plants took 1 d longer and were smaller compared with those from susceptible plants. This study suggests that biological control by B. communis may be compromised when host plant resistance is widely used for pest management of soybean aphids.

Insect-damaged corn stalks decompose at rates similar to Bt-protected, non-damaged corn stalks

The relative decomposability of corn (Zea mays L.) residues from insect (Bt)-protected hybrids and conventional hybrids cultivated under insect pressure was investigated in two studies. Above-ground biomass, residue macromolecular composition, and stalk physical strength were also measured. In the first decomposition study, chopped residues (stalks and leaves) were used from a corn rootworm-protected (Cry3Bb1) hybrid and its non-Bt near isoline that were grown in replicated plots infested with corn rootworms (Diabrotica spp.). In the second study, residue (intact stalk sections) was used from three European corn borer (ECB, Ostrinia nubilalis Hübner)-resistant (Cry1Ab) hybrids representing different seed manufacturer/maturity date series, their non-Bt near isolines, two Cry3Bb1-protected isolines, and three additional conventional hybrids, all cultivated in replicated plots under conditions of elevated ECB pressure. In both studies, insect-resistant residues decomposed at rates similar to their non-protected near isolines. No evidence was found that insect-protected hybrids produced more above-ground biomass or had distinct residue composition. While some measures of mechanical stalk strength indicated that ECB-damaged stalks were not as stiff as protected stalks, these physical differences did not translate into differences in residue decomposition. We conclude that while individual hybrids may vary in their production of biomass, residue composition or residue decomposability, these characteristics do not systematically vary with the presence of the Bt gene conferring insect resistance, even under conditions of insect pressure.

Factors Contributing to the Poor Performance of a Soybean Aphid Parasitoid Binodoxys communis (Hymenoptera: Braconidae) on an Herbivore Resistant Soybean Cultivar

ABSTRACT Host plant resistance and biological control are important components of integrated pest management programs. However, plants expressing resistance to herbivores may also have direct or indirect negative effects on natural enemies simultaneously providing pest suppression. Soybean aphids (Aphis glycines Matsumura) are invasive and serious pests of soybean (Glycine max L.) in the United States. Several soybean lines with aphid resistance have been identified, but the long-term impact of these resistant plants on soybean aphid biological control agents is uncertain. In a previous study, we reported that a soybean aphid parasitoid, Binodoxys communis (Gahan) had lower mummy production on resistant plants compared with a near isogenic susceptible soybean line, but the reason for this was unclear. Therefore, we examined three possible mechanisms to explain these findings: 1) resistant plants directly impact wasp emergence and longevity, 2) varying aphid density influences parasitism rates, and 3) resistant plants indirectly affect wasp development through reduced aphid longevity. We found that parasitoids in this study were not directly influenced by resistant cultivais, as there was no difference in wasp adult emergence or longevity between resistant and susceptible plants. There was also no significant effect of aphid density on mummy production over the range of aphid densities we tested. However, aphids on resistant plants had significantly shorter lifespans and were unable to survive long enough to develop into mummies compared with aphids on susceptible plants. We discuss these results and possible implications for integrating biological control and host plant resistance within soybean aphid integrated pest management programs.

Integrated Management of Canada Thistle (Cirsium arvense) with Insect Biological Control and Plant Competition under Variable Soil Nutrients

Abstract Because of economic and environmental constraints, alternatives to chemical management of Canada thistle (Cirsium arvense) are frequently sought, but adequate nonchemical suppression of this invasive species remains elusive. Combining biological control with other tactics may be an effective approach to suppress Canada thistle, but more information is needed about how environmental conditions affect interspecific interactions. We investigated effects of a biocontrol agent (Hadroplontus litura, a stem-mining weevil) and a potential plant competitor (common sunflower, Helianthus annuus, native annual) on Canada thistle under two soil nutrient regimes in outdoor microcosms. Larval mining damage was relatively light, and weevils negatively impacted only main shoot height and flower number. All measures of Canada thistle performance were reduced when plants were grown with common sunflower or in reduced nutrients, although effects of the latter on root biomass were not significant. Effects of common sunflower and soil nutrients on Canada thistle were generally additive, though a marginally insignificant interaction indicated a trend for greatest flower number with high nutrients and absence of common sunflower. Effects of weevils and common sunflower on Canada thistle were also additive rather than interactive. Although larval damage ratings were significantly greater on plants grown in high-nutrient soil, under our experimental conditions weevils and soil nutrients did not have a significant interactive effect on Canada thistle plants. Our results indicate that H. litura is a relatively weak biological control agent, but when combined with competitive desirable vegetation, some level of Canada thistle suppression may be possible, especially if soil nutrient levels are not highly enriched from agricultural runoff. Assessing the true ecological impacts of Canada thistle infestations may be an important direction for future research. Nomenclature: Stem-mining weevil, Hadroplontus litura Fabricius, Canada thistle, Cirsium arvense (L.) Scop., common sunflower, Helianthus annuus L. Management Implications: Canada thistle is a problematic invasive plant in many temperate regions of the northern hemisphere, and management continues to be a challenge. Research suggests that integrating multiple control tactics enhances suppression of Canada thistle, but that effects often depend on environmental context. In our microcosm study, weevil herbivory, common sunflower competition, and reduced levels of soil nutrients had substantial negative effects on many measures of Canada thistle growth and reproductive capacity. Overall, the latter two factors exerted the strongest negative effects; however, weevil damage was generally light. Canada thistle grown in high-nutrient soils had greater main-stem biomass, numbers of side shoots, and numbers of flowers, even though larval stem-mining damage was greater for these plants. Common sunflower proved to be a good competitor against Canada thistle, and sowing this type of fast-growing annual forb, which occupies a similar soil niche to Canada thistle, alongside perennial native plants (e.g., competitive grasses) may enhance restoration outcomes.

Corn Earworms (Lepidoptera: Noctuidae) as Pests of Soybean

Corn earworm Helicoverpa zea (Boddie) is a well-known pest of corn and cotton, but can also be problematic in soybean, particularly in the southern United States. Their preference for reproductive structures of the soybean plant can dramatically impact yield, particularly when infestations occur during early reproductive plant growth stages. We discuss the life history, ecology, plant damage, and management of H. zea as it relates to soybean production.

Predicting Developmental Timing for Immature Canada Thistle Stem-Mining Weevils, Hadroplontus litura (Coleoptera: Curculionidae)

ABSTRACT Predictions of phenological development for insect biological control agents may facilitate post-release monitoring efforts by allowing land managers to optimize the timing of monitoring activities. A logistic thermal time model was tested to predict phenology of immature stem-mining weevils, Hadroplontus litura F. (Coleoptera: Curculionidae), a biological control agent for Canada thistle, Cirsium arvense L. (Asterales: Asteraceae). Weevil eggs and larvae were collected weekly from Canada thistle stems in eastern North Dakota from May through July during 2010 and 2011. Head capsule widths of sampled larvae were measured at the widest point and plotted on a frequency histogram to establish ranges of head capsule widths associated with each instar.We found head capsule width ranges for first-, second-, and third-instar H. litura larvae were 165–324 µm, 346–490µmm, and 506–736 µm, respectively. Logistic regression models were developed to estimate the proportions of H. litura eggs, first-, and second-instar larvae in the weevil population as a function of thermal time. Model estimates of median development time for eggs, first instars, and second instars ranged from 219 ± 23 degree-days (DD) to 255 ± 27 DD, 556 ± 77 DD to 595 ± 81 DD, and 595 ± 109 DD to 653 ± 108 DD, respectively. Based on model validation statistics, model estimates for development timing were the most accurate for eggs and first instars and somewhat less accurate for second instars. These model predictions will help biological control practitioners obtain more accurate estimates of weevil population densities during postrelease monitoring.

Reproduction of Soybean Aphid (Hemiptera: Aphididae, Aphis glycines Matsumura) on Clover (Trifolium spp.)

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is native to Asia and has spread throughout the north central United States since it was first reported in Wisconsin in 2000 (Alleman, 2002; Venette, 2004). Since this time A. glycines has had a profound impact on soybean production, both by its potential to decrease yield up to 40% (Ragsdale et al., 2007) and by increasing production costs via increased scouting and pesticide applications (Song and Swinton, 2009). Aphis glycines is a typical heteroecious holocyclic aphid species and is associated with a narrow range of host plants (Blackman and Eastop, 1994, 2000). To date, confirmed primary hosts in North America are Rhamnus cathartica L., R.alnifolia L’Hér., and R. lanceolata Pursh. (Voegtlin et al., 2004, 2005; Yoo et al., 2005). Primary hosts are where eggs overwinter and hatch in the spring. Newly hatched nymphs develop into fundatrices (stem mothers) that produce a second generation, which primarily consist of wingless (apterous) females (Ragsdale et al., 2004). The third and following generations produced on Rhamnus spp. will primarily be winged (alate) females that emigrate to secondary hosts and reproduce asexually. Although specialist heteroecious aphid species are associated with a limited number of secondary plant hosts, they often settle and feed on a variety of plant species during spring migration. However, these may not support reproduction and are not necessarily considered hosts (Blackman and Eastop, 2000; Alleman et al., 2002; Hill et al., 2004; Ragsdale et al., 2004). Aphis glycines primarily use soybean (Glycine max L.) and wild Glycine species as secondary hosts, although studies indicate they can colonize other species within the Fabaceae, notably clover (Trifolium spp.; Alleman et al., 2002; Hill et al., 2004). These alternate plant hosts can potentially facilitate pest invasions by serving as temporal bridges that sustain aphid populations prior to the availability of soybeans (Voegtlin et al., 2005; Clark et al., 2006). Clover is common in the landscape and has a cosmopolitan distribution. Several species, especially varieties of red and white clover, are commonly used as cover crops as well as for forage, grazing and silage. Primary growth of clover occurs early in spring, and average first flowering date takes place in midMay (Ayres et al., 1998; Williams and Abberton, 2004) well before the time of initial movement of A. glycines into soybean, which occurs between early June and late July (Ragsdale et al., 2007). Another possible consequence of alternate host use by A. glycines is enhanced transmission of plant viruses to soybeans (Hill et al., 2004). Many aphids can rapidly acquire viruses by merely probing the epidermal tissue of an infected plant with their stylets (Dixon, 1973). Aphis glycines can transmit soybean mosaic, cucumber mosaic and alfalfa mosaic virus, diseases which may also be present in clover (Šutić et al., 1999; Hill et al., 2001, 2004; Alleman et al., 2002). Previous studies of A. glycines reproduction on clover assessed a limited number of Trifolium varieties (Alleman et al., 2002; Hill et al., 2004). In this study we quantified A. glycines densities on four varieties of red clover (T. pratense L.; Arlington, Mammoth, Medium Red, Starfire), three varieties of white clover (T. repens L.; Kopu II, Ladino, Pitau), a hybrid of red and white clover (T. hybridum L.; Alsike), berseem clover (T. alexandrinum L.) and crimson clover (T. incarnatum L.). We also examined if nitrogen content and biomass of above-ground plant tissue affected densities of apterous and alate aphids.

Soybean Aphid Response to their Alarm Pheromone E-ß-Farnesene (EBF)

When attacked by natural enemies some insect pests, including many aphid species, alert neighboring conspecifics with alarm pheromones. Cornicle secretions with pheromones benefit the attacked aphid but are costly to produce, while alarm pheromone benefits probably fall largely on alerted conspecifics. Given these variable benefits, the likelihood of a secretion may change depending on aphid density. Thus, we first hypothesized that the common alarm pheromone in aphids, E-ß-farnesene (EBF), was present in soybean aphid (Aphis glycines Matsumura) cornicle secretions and would elicit an alarm response in aphids exposed to it. Second, since aphids other than the secretor also benefit from cornicle secretions, we hypothesized that the likelihood of secretion would increase concurrently with the density of neighboring clonal conspecifics. Third, because alarm reaction behavior (e.g. feeding cessation) is probably costly, we hypothesized that alarm reaction behavior would decrease as conspecific density (i.e. alternative prey for an attacking natural enemy) increased. We found that soybean aphids 1) produce cornicle secretions using EBF as an alarm pheromone, 2) are less likely to release cornicle secretions when alone than in a small group (~10 individuals), but that the rate of secretion does not increase further with additional conspecific density, and 3) also exhibit alarm reaction behavior in response to cornicle secretions independent of aphid density. We show that soybean aphids can use their cornicle secretions to warn their neighbors of probable attack by natural enemies, but that both secretion and alarm reaction behavior does not change as density of nearby conspecifics rises above a few individuals.

Tracking predation of subterranean pests: digestion of corn rootworm DNA by a generalist mite

qPCR is a useful tool for understanding predator–prey relationships. We investigated rootworm DNA digestion by male and female predatory mites. Males and females initially consumed comparable amounts of DNA, which was digested at similar rates. Field-collected mites need to be preserved quickly for best qPCR results.

Life History and Phenology of an Endophagous Stem-Mining Herbivore (Coleoptera: Curculionidae, Hadroplontus litura) of a Clonal Weed

Abstract Herbivorous insects can be an important part of weed management, but it is necessary to understand the life history of the organisms involved and how they interact. This is especially pertinent when dealing with endophagous insects with restricted mobility. Hadroplontus litura F. is a stem-mining weevil that is considered a biological control agent of Canada thistle (Cirsium arvense L.), a perennial weed that forms clonal networks. We investigated the biology of H. litura and its association with Canada thistle at six field sites along a latitudinal gradient over 2 yrs, including documenting immature phenology and feeding damage, quantifying immature life stages, and exploring relationships between weevils and shoot size as well as weevil density and feeding damage. Eggs were present until the beginning of June and third-instar larvae began to exit shoots in mid-June, although some were present in July. It appeared that adult females laid more eggs on larger shoots, and preferred shoots not previously used for oviposition. The head capsule size of third instars was not correlated with shoot size, but it was positively related to larval density. Overall, infested shoots had an average of four weevil immatures, although densities ranged up to 21. Larval density was positively associated with stem damage, and both parameters appeared to be more intense at our sites than previous reports. Understanding how the intensity of larval damage impacts Canada thistle plants over time is critical to understanding the relevance of these insects for weed biocontrol.