Christine A. Bahlai

Modeling Distribution and Abundance of Soybean Aphid in Soybean Fields Using Measurements From the Surrounding Landscape

ABSTRACT Soybean aphid (Aphis glycines Matsumura) is a severe pest of soybean in central North America. Outbreaks of the aphid in Ontario are often spotty in distribution, with some geographical areas affected severely and others with few or no aphid populations occurring in soybean for the duration of the season. A. glycines spend summers on soybean and overwinter on buckthorn, a shrub that is widespread in southern Ontario and is commonly found in agricultural hedgerows and at the margins of woodlots. A. glycines likely use both short distance migratory flights from buckthorn and longer distance dispersal flights in the search for acceptable summer hosts. This study aims to model colonization of soybean fields by A. glycines engaged in early-season migration from overwintering hosts. Akaikes information criterion (AIC) was used to rank numerous competing linear and probit models using field parameters to predict aphid presence, colonization, and density. The variable that best modeled aphid density in soybean fields in the early season was the ratio of buckthorn density to field area, although dramatic differences in relationships between the parameters were observed between study years. This study has important applications in predicting areas that are at elevated risk of developing economically damaging populations of soybean aphid and which may act as sources for further infestation.

Predation by Coccinella septempunctata and Harmonia axyridis (Coleoptera: Coccinellidae) on Aphis glycines (Homoptera: Aphididae)

ABSTRACT Coccinella septempunctata L. and Harmonia axyridis Pallas are key natural enemies of soybean aphid, Aphis glycines Matsumura, in North America. Third instars, adult females, and adult males of both C. septempunctata and H. axyridis exhibited a type II functional response for predation toward adult soybean aphids at 26 ± 1°C. In C. septempunctata, the functional response curve of adult males differed from those of third instars and adult females, but there was no difference between third instars and adult females. In H. axyridis, the functional response curves of larvae, adult females, and adult males all differed significantly. Third instars and adult females consumed significantly more soybean aphids than did adult males at prey densities of 150 and 180 aphids per arena for C. septempunctata and at prey densities of 60, 90, 120, 150, and 180 aphids per arena for H. axyridis. The theoretical maximum daily predation rate of adult aphids by C. septempunctata was predicted to be 204 per third instar, 277 per adult female, and 166 per adult male, and 244, 156, and 73, respectively, for H. axyridis. Third instars and adult females of both species consumed significantly more aphids than did adult males on soybean plants with the recommended action threshold of 250 soybean aphids per plant. Both C. septempunctata and H. axyridis have high predation capacities and are important in suppressing soybean aphid populations.

Role of Visual and Olfactory Cues from Agricultural Hedgerows in the Orientation Behavior of Multicolored Asian Lady Beetle (Coleoptera: Coccinellidae)

Abstract Harmonia axyridis Pallas is an introduced lady beetle common in eastern North American agroecosystems. Two-choice behavioral bioassays were performed to determine whether visual and olfactory stimuli from prey and host habitats could elicit taxis in wild-collected H. axyridis adults and whether beetles exhibit a preference among stimuli. Soybean aphid (Aphis glycines Matsumura) spends much of the year in agricultural hedgerows residing on buckthorn (Rhamnus cathartica L), and H. axyridis is frequently observed feeding on aphids in this habitat. Olfactory bioassays were performed in a Y-tube olfactometer and tested the response of beetles to the odor of buckthorn leaves, apple leaves (Malus domestica Borkh.), and buckthorn leaves both naturally and artificially infested with A. glycines. No differences were observed between the numbers of beetles moving toward the odor of buckthorn artificially infested with A. glycines and uninfested buckthorn, but more beetles preferred naturally infested buckthorn over uninfested buckthorn. Visual bioassays were performed in an acrylic tube arena,and tested beetle response to silhouettes and to apple and buckhorn leaves. Beetles were significantly more likely to choose silhouettes over blank space in visual trials. Significantly more beetles moved toward buckthorn leaves than blank space, but beetles did not discern between apple and buckthorn until olfactory cues were also included. This study lays the foundation for future work examining the response of H. axyridis to visual and olfactory cues in Ontario agroecosystems, which could help enhance effectiveness of H. axyridis as a biological control and mitigate its impacts as a pest species.

The role of exotic ladybeetles in the decline of native ladybeetle populations: evidence from long-term monitoring

Ladybeetles (Coleoptera: Coccinellidae) are ubiquitous predators which play an important role in suppressing pest insects. In North America, the coccinellid community is increasingly dominated by exotic species, and the abundance of some native species has declined dramatically since the 1980s. Several hypotheses have been proposed to describe the mechanism of invasion coupled with native species declines, e.g. vacant niche exploitation, intraguild predation, competitive exploitation and habitat compression. We analyze a 24-year dataset of coccinellid community structure in southwestern Michigan to elucidate the most likely mechanism(s) of native coccinellid decline and implications for their conservation. Correlation analyses indicated that impact of exotic species on native coccinellids varies with their degree of interaction. Although several native species were observed to be in numerical decline, only Adalia bipunctata and Coleomegilla maculata had declines that were statistically significant. The magnitude of decline in these two species varied with the degree of dietary overlap with invaders, thus their decline is most likely driven by competitive exploitation. Habitat use patterns by some native species (A. bipunctata and Coccinella trifasciata) changed during years when the exotic Harmonia axyridis reached high numbers, lending support to the habitat compression hypothesis, where native species survive in ancestral (i.e. natural or semi-natural) habitats when invaders dominate cultivated habitats. Coccinellid communities occurring in semi-natural forested habitats were unique in both composition and variability from those occurring in cultivated habitats. Such semi-natural habitats can act as refuges for native coccinellids and may play a role in maintaining the functional resilience of coccinellid communities.

Decline of Soybean Aphid (Homoptera: Aphididae) Egg Populations from Autumn to Spring on the Primary Host, Rhamnus cathartica

Abstract Soybean aphid, Aphis glycines Matsumura (Homoptera: Aphididae), is a severe pest of soybeans in North America. Soybean aphid populations cycle between a secondary summer host, where populations reproduce parthenogenetically and a primary host, where populations overwinter as eggs. In North America, the secondary host is soybean, and the primary hosts are Rhamnus cathartica L. (Rhamnaceae) and R. alnifolia L’Her. A location with abundant populations of soybean aphid on R. cathartica was identified near Guelph, Ontario, Canada, in October 2004, and eggs on trees were counted at multiple sites within that location each autumn and spring over the next 2 yr. Dynamics of naturally occurring soybean aphid populations on the primary host were assessed with respect to (1) decline of overwintering eggs from autumn to spring, (2) development of spring populations on R. cathartica, and (3) development of soybean aphid populations on soybean immediately adjacent to overwintering sites. Counts of aphid eggs declined by ≈70% between autumn and spring sampling periods in 2004–2005. Significant differences in counts of aphid eggs relative to sampling height were observed in the canopy of R. cathartica. No edge effects were observed in the development of soybean aphid populations in soybeans adjacent to overwintering sites in this study. Very few eggs were collected at the same study location in the autumn of 2005, and no aphid eggs were collected from samples taken in the spring of 2006. Egg counts taken in the autumn of 2006 were intermediate in number relative to counts taken in the autumn of 2004 and 2005.

Incorporating natural enemy units into a dynamic action threshold for the soybean aphid, Aphis glycines (Homoptera: Aphididae)

BACKGROUND Recommended action thresholds for soybean aphid, Aphis glycines, do not adjust for natural enemy impact, although natural enemies contribute important biological control services. Because individual natural enemy species have varied impacts on pest population dynamics, incorporating the impact of a diverse predator guild into an action threshold can be cumbersome. RESULTS Field surveys identified an aphidophagous natural enemy complex dominated by Orius insidiosus, Coccinella septempunctata, Harmonia axyridis and Aphelinus certus. Functional responses of O. insidiosus were determined in the laboratory, while predation rates of all other natural enemies were obtained from the literature. Natural enemy impacts were normalized using natural enemy units (NEUs), where 1 NEU = 100 aphids consumed or parasitized. A dynamic action threshold (DAT) was developed by combining NEUs with an A. glycines population growth model. With the DAT, an insecticide application was only triggered if natural enemy numbers were insufficient to suppress pest populations. In field experiments, DAT provided equivalent yields to the conventional action threshold and reduced the average number of pesticide applications. CONCLUSION The DAT approach has the potential to reduce pesticide use, will help preserve natural enemy populations and can be applied to other pest systems with diverse natural enemy guilds.

Shifts in dynamic regime of an invasive lady beetle are linked to the invasion and insecticidal management of its prey

The spread and impact of invasive species may vary over time in relation to changes in the species itself, the biological community of which it is part, or external controls on the system. We investigate whether there have been changes in dynamic regimes over the last 20 years of two invasive species in the midwestern United States, the multicolored Asian lady beetle Harmonia axyridis and the soybean aphid Aphis glycines. We show by model selection that after its 1993 invasion into the American Midwest, the year-to-year population dynamics of H. axyridis were initially governed by a logistic rule supporting gradual rise to a stable carrying capacity. After invasion of the soybean aphid in 2000, food resources at the landscape level became abundant, supporting a higher year-to-year growth rate and a higher but unstable carrying capacity, with two-year cycles in both aphid and lady beetle abundance as a consequence. During 2005-2007, farmers in the Midwest progressively increased their use of insecticides for managing A. glycines, combining prophylactic seed treatment with curative spraying based on thresholds. This human intervention dramatically reduced the soybean aphid as a major food resource for H. axyridis at landscape level and corresponded to a reverse shift towards the original logistic rule for year-to-year dynamics. Thus, we document a short episode of major predator-prey fluctuations in an important agricultural system resulting from two biological invasions that were apparently damped by widespread insecticide use. Recent advances in development of plant resistance to A. glycines in soybeans may mitigate the need for pesticidal control and achieve the same stabilization of pest and predator populations at lower cost and environmental burden.

Generalist Predators (Coleoptera: Carabidae, Staphylinidae) Associated with Millipede Populations in Sweet Potato and Carrot Fields and Implications for Millipede Management

ABSTRACT The predatory beetle assemblage of Ontario carrot and sweet potato fields was described and assessed to identify species of interest to the control of the emerging pest millipede Cylindroiulus caeruleocinctus (Wood) (Diplopoda: Julidae). Pterostichus melanarius (Coleoptera: Carabidae) was identified as a dominant species, and seven other carabid species [Pterostichus melanarius (Illiger), Harpalus pensylvanicus (DeGeer), Ophonus puncticeps (Stephens), H. erraticus Say, Bembidion quadrimaculatum oppositum Say, Poecilus chalcites (Say), Scarites subterraneus Fabricius, and Pterostichus permundus (Say)] were identified as common species on the basis of activity density. Common species became more abundant as the growing season progressed. In laboratory bioassays, P. melanarius preyed on millipedes regardless of prey size, whereas H. erraticus never selected millipedes as prey. A significant positive spatiotemporal relationship was found between P. melanarius and C. caeruleocinctus in sweet potato fields. P. melanarius was found to be a natural enemy of C. caeruleocinctus, and other common carabid species warrant future study. The role of Staphylinidae in millipede control could not be elucidated, likely because of low trapping efficiency. Tachinus corticinus Gravenhorst, an introduced staphylinid from Europe, was newly recorded in Ontario, extending its North American range considerably westward from the province of Quebec. The results of this study are an important foundational step toward developing a successful integrated pest management strategy for controlling millipede damage in crops.

Development of Soybean Aphid (Homoptera: Aphididae) on Its Primary Overwintering Host, Rhamnus cathartica

Abstract Thermally dependent development of soybean aphid (Aphis glycines Matsumura) and common buckthorn (Rhamnus cathartica L.) were examined in growth chambers in spring 2005. Models based on ambient air temperatures for all development events were developed. Adjusted models were developed to account for heat units acquired because of solar radiation. These models were tested at field sites in Guelph and Ridgetown, Ontario, Canada. It was found that egg hatch of aphids and bud swell of buckthorn coincided at low temperatures in growth chambers and in the field. Development thresholds of 9 and 10°C were acquired for bud swell and egg hatch, respectively. Models based on ambient air temperatures were poor predictors of bud swell and egg hatch in the field, but models adjusted for solar radiation predicted these events just 1–4 d before they were observed at both sites. The results obtained have broad application for predicting aphid hatch on a regional basis.

The Role of Natural Enemy Foraging Guilds in Controlling Cereal Aphids in Michigan Wheat

Insect natural enemies (predators and parasitoids) provide important ecosystem services by suppressing populations of insect pests in many agricultural crops. However, the role of natural enemies against cereal aphids in Michigan winter wheat (Triticum aestivum L.) is largely unknown. The objectives of this research were to characterize the natural enemy community in wheat fields and evaluate the role of different natural enemy foraging guilds (foliar-foraging versus ground-dwelling predators) in regulating cereal aphid population growth. We investigated these objectives during the spring and summer of 2012 and 2013 in four winter wheat fields on the Michigan State University campus farm in East Lansing, Michigan. We monitored and measured the impact of natural enemies by experimentally excluding or allowing their access to wheat plants infested with Rhopalosiphum padi (L.) and Sitobion avenae (F.) (Hemiptera: Aphidae). Our results indicate that the natural enemy community in the wheat fields consisted mostly of foliar-foraging and ground-dwelling predators with relatively few parasitoids. In combination, these natural enemy groups were very effective at reducing cereal aphid populations. We also investigated the role of each natural enemy foraging guild (foliar-foraging versus ground-dwelling predators) independently. Overall, our results suggest that, in combination, natural enemies can almost completely halt early-season aphid population increase. Independently, ground-dwelling predators were more effective at suppressing cereal aphid populations than foliar-foraging predators under the conditions we studied. Our results differ from studies in Europe and the US Great Plains where foliar foraging predators and parasitoids are frequently more important cereal aphid natural enemies.