Robert J. O’Neil

Soybean Aphid Biology in North America

Abstract Soybean aphid, Aphis glycines Matsumura, a native of eastern Asia, was first discovered in North America in July 2000 in Wisconsin and subsequently in a total of 10 North Central U.S. states by September 2000. Currently, soybean aphid has spread to 20 U.S. states and three Canadian provinces, putting >60 million acres of soybean at risk to crop injury caused by this exotic insect. The life history of this species has been studied by a number of entomologists and crop protection specialists, and here we provide a summary of the observations made by ourselves and our colleagues. The soybean aphid has been observed at all stages of a heterecious holocyclic life cycle and seems to be adapting to a large geographic area of the North Central United States. Soybean aphid uses native and exotic primary hosts found in North America, specifically Rhamnus cathartica L. and Rhamnus alnifolia L’Hér. The aphid’s principal secondary host is soybean, Glycine max (L.) Merr., but there seems to be a lengthy gap in early spring between the production of alatae on buckthorn (Rhamnus spp.) and the occurrence of soybean. In the fall when soybean is senescing, a biological bottleneck is created as the aphid must develop sexual morphs on soybean that emigrate back to the primary host to complete the sexual phase of its life cycle. During the summer, A. glycines is prone to develop winged morphs during any generation on soybean, which puts much of the soybean crop at risk of invasion by this exotic species, even if the insect does not overwinter locally. The integrated pest management challenges presented by the aphid require a deeper understanding of its biology as it adapts to North America.

Soybean Aphid Predators and Their Use in Integrated Pest Management

Abstract The discovery of the soybean aphid, Aphis glycines Matsumura, in U.S. soybean production systems in 2000 has provided a unique opportunity to study the interaction of a new invader with existing natural enemy communities. One research thrust has been examining the role of predators in soybean aphid dynamics in the Midwest. We discuss the roles of predatory arthropods in field crops and set forth a conceptual model that we have followed to identify key predators in the soybean aphid system. We identify Orius insidiosus (Say) and Harmonia axyridis (Pallas) as potentially key predators and show our findings on their phenology in soybean fields and their impact on soybean aphid population dynamics. Finally, we discuss how this information can be used in integrated pest management programs for soybean aphid and point to gaps in our knowledge where future studies are needed.

Tracking the role of alternative prey in soybean aphid predation by Orius insidiosus: a molecular approach

The soybean aphid, Aphis glycines (Hemiptera: Aphididae), is a pest of soybeans in Asia, and in recent years has caused extensive damage to soybeans in North America. Within these agroecosystems, generalist predators form an important component of the assemblage of natural enemies, and can exert significant pressure on prey populations. These food webs are complex and molecular gut‐content analyses offer nondisruptive approaches for examining trophic linkages in the field. We describe the development of a molecular detection system to examine the feeding behaviour of Orius insidiosus (Hemiptera: Anthocoridae) upon soybean aphids, an alternative prey item, Neohydatothrips variabilis (Thysanoptera: Thripidae), and an intraguild prey species, Harmonia axyridis (Coleoptera: Coccinellidae). Specific primer pairs were designed to target prey and were used to examine key trophic connections within this soybean food web. In total, 32% of O. insidiosus were found to have preyed upon A. glycines, but disproportionately high consumption occurred early in the season, when aphid densities were low. The intensity of early season predation indicates that O. insidiosus are important biological control agents of A. glycines, although data suggest that N. variabilis constitute a significant proportion of the diet of these generalist predators. No Orius were found to contain DNA of H. axyridis, suggesting intraguild predation upon these important late‐season predators during 2005 was low. In their entirety, these results implicate O. insidiosus as a valuable natural enemy of A. glycines in this soybean agroecosystem.

Suppression of Population Growth of the Soybean Aphid, Aphis glycines Matsumura, by Predators: The Identification of a Key Predator and the Effects of Prey Dispersion, Predator Abundance, and Temperature

Abstract The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), has recently invaded North America from Asia and has become a major pest in soybean. Using field surveys and cage exclusion techniques, we identified the effect of natural enemies and abiotic factors on the growth of soybean aphid populations in 2004 and 2005. The soybean aphid population was significantly limited by natural enemies in the field. Generalist predators dominated the natural enemy community. One species, Orius insidiosus Say (Hemiptera: Anthocoridae) represented 85–90% of predators found. There was a significant negative relationship between aphid population growth and O. insidiosus abundance. For other predators, there were no relationships between abundance and aphid population growth. The spatial distribution of aphids among plants affected the impact of O. insidiosus on aphid population growth. When aphids were distributed in a clumped manner, increases in O. insidiosus numbers resulted in lower aphid growth rates. For randomly distributed aphids, there was no effect of O. insidiosus abundance on aphid population growth. Finally, we found no relationship between aphid population growth and degree-day accumulations. The potential of O. insidiosus to suppress soybean aphid population growth at low aphid numbers and the importance of the predator to soybean aphid integrated pest management are discussed.

Prospects for Importation Biological Control of the Soybean Aphid: Anticipating Potential Costs and Benefits

Abstract We discuss the potential pros and cons of using importation biological control against the soybean aphid, Aphis glycines Matsumura (Homoptera: Aphididae). Importation of exotic organisms for biological control is never completely risk-free, but the potential negative impacts of not achieving biological control of invasive pests may exceed the risks associated with a biological control introduction. The potential benefits of biological control include reduced insecticide use and a reduced ability of the invasive pest to impact native flora and fauna, and we outline what the scope of these benefits may be for the soybean aphid. The benefits are only accrued, however, if biological control is successful, so the likelihood of successful biological must also be assessed. Accordingly, we outline some issues relevant to predicting the success of importation biological control of the soybean aphid. We also outline the potential risks to nontarget organisms that would be associated with importation biological control of the soybean aphid. Currently, two parasitoid species, Aphelinus albipodus Hayat and Fatima (Hymenoptera: Aphelinidae) and Lipolexis gracilis Förster (Hymenoptera: Braconidae) have been imported from Asia and have passed through quarantine. We briefly review the biology and host range of these two species. A different strain of A. albipodus that was released against the Russian wheat aphid, Diuraphis noxia (Mordvilko) (Homoptera: Aphididae), in the early 1990s was also found to attack the soybean aphid in the laboratory and has been redistributed from Wyoming to Minnesota and Wisconsin in field releases against the soybean aphid. We discuss our rationale for going forward with this redistribution.

Differential impact of adults and nymphs of a generalist predator on an exotic invasive pest demonstrated by molecular gut-content analysis

Generalist predators have the capacity to regulate herbivore populations through a variety of mechanisms, but food webs are complex and defining the strength of trophic linkages can be difficult. Molecular gut-content analysis has revolutionized our understanding of these systems. Utilizing this technology, we examined the structure of a soybean food web, identified the potential for adult and immature Orius insidiosus (Hemiptera: Anthocoridae) to suppress Aphis glycines (Hemiptera: Aphididae), and tested the hypotheses that foraging behaviour would vary between life stages, but that both adults and immatures would exert significant predation pressure upon this invasive pest. We also identified the strength of trophic pathways with two additional food items: an alternative prey item, Neohydatothrips variabilis (Thysanoptera: Thripidae), and an intraguild predator, Harmonia axyridis (Coleoptera: Coccinellidae). A. glycines constituted a greater proportion of the diet of immature O. insidiosus, but N. variabilis DNA was found in greater frequency in adults. However, both life stages were important early-season predators of this invasive pest, a phenomenon predicted as having the greatest impact on herbivore population dynamics and establishment success. No adult O. insidiosus screened positive for H. axyridis DNA, but a low proportion (2.5%) of immature individuals contained DNA of this intraguild predator, thus indicating the existence of this trophic pathway, albeit a relatively minor one in the context of biological control. Interestingly, approximately two-thirds of predators contained no detectable prey and fewer than 3% contained more than one prey item, suggesting the possibility for food limitation in the field. This research implicates O. insidiosus as a valuable natural enemy for the suppression of early-season A. glycines populations.

Defensive Response of Soybean Aphid (Hemiptera: Aphididae) to Predation by Insidious Flower Bug (Hemiptera: Anthocoridae)

Abstract During research on the life history characteristics of insidious flower bug, Orius insidiosus (Say), fed soybean aphids, Aphis glycines Matsumura, the mouthparts of some predators were covered by a substance excreted from the cornicles of attacked aphids. The cornicle exudate was found to encumber both nymphs and adults of O. insidiosus causing death because of molting failure and starvation. Among predator stages, first instars were most severely affected. Feeding frequency affected the number of predators affected by the exudate, with predators fed more often having higher rates of exudate exposure and mortality. Soybean aphids produce exudate during all life stages, and its production does not seem to compromise the survival of the aphid. The exudate also seems to contain an alarm pheromone as evidenced by increased movement and activity of aphids in the vicinity of exudate-producing aphids. The potential impact of the aphid’s cornicle defenses on aphid–predator dynamics in soybean, Glycine max (L.) Merr., is discussed.

Effects of Meteorological Variation on Mortality in Populations of the Spittlebug Deois flavopicta (Homoptera: Cercopidae)

Abstract We found that variation in temperature and humidity significantly affected mortality rates and population dynamics of the spittlebug Deois flavopicta Stål by monitoring cohorts of diapausing eggs and nymphs for three generations. Cohorts of quiescent eggs, when exposed to increasing periods of high moisture (free water), produced higher proportions of eggs resuming embryonic development in laboratory experiments. The accumulated number of eggs resuming development as a function of days of exposure to moist conditions was modeled using a β distribution. Periods of drought and high temperatures after the beginning of postdiapause development increased embryonic and nymphal mortality. Mortality was modeled with a linear function, and in combination with the development model allowed the simulation of varying mortality rates in the newly emerged nymphal population. Comparisons with field data demonstrated a close fit to the observed and expected proportion of nymphs hatching daily. By accurately simulating natural mortality, hatching distribution and population dynamics, the model promises to be useful for managing the spittlebug in the field.