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Ecological Applications | 2009

Landscape diversity enhances biological control of an introduced crop pest in the north-central USA

M. M. Gardiner; Douglas A. Landis; Claudio Gratton; Christina DiFonzo; Matthew E. O'Neal; J. M. Chacon; M. T. Wayo; N. Schmidt; E. E. Mueller; George E. Heimpel

Arthropod predators and parasitoids provide valuable ecosystem services in agricultural crops by suppressing populations of insect herbivores. Many natural enemies are influenced by non-crop habitat surrounding agricultural fields, and understanding if, and at what scales, land use patterns influence natural enemies is essential to predicting how landscape alters biological control services. Here we focus on biological control of soybean aphid, Aphis glycines Matumura, a specialist crop pest recently introduced to the north-central United States. We measured the amount of biological control service supplied to soybean in 26 replicate fields across Michigan, Wisconsin, Iowa, and Minnesota across two years (2005-2006). We measured the impact of natural enemies by experimentally excluding or allowing access to soybean aphid infested plants and comparing aphid population growth over 14 days. We also monitored aphid and natural enemy populations at large in each field. Predators, principally coccinellid beetles, dominated the natural enemy community of soybean in both years. In the absence of aphid predators, A. glycines increased significantly, with 5.3-fold higher aphid populations on plants in exclusion cages vs. the open field after 14 days. We calculated a biological control services index (BSI) based on relative suppression of aphid populations and related it to landscape diversity and composition at multiple spatial scales surrounding each site. We found that BSI values increased with landscape diversity, measured as Simpsons D. Landscapes dominated by corn and soybean fields provided less biocontrol service to soybean compared with landscapes with an abundance of crop and non-crop habitats. The abundance of Coccinellidae was related to landscape composition, with beetles being more abundant in landscapes with an abundance of forest and grassland compared with landscapes dominated by agricultural crops. Landscape diversity and composition at a scale of 1.5 km surrounding the focal field explained the greatest proportion of the variation in BSI and Coccinellidae abundance. This study indicates that natural enemies provide a regionally important ecosystem service by suppressing a key soybean pest, reducing the need for insecticide applications. Furthermore, it suggests that management to maintain or enhance landscape diversity has the potential to stabilize or increase biocontrol services.


Annals of The Entomological Society of America | 2008

Aphidophagous Predators in Iowa Soybean: A Community Comparison across Multiple Years and Sampling Methods

Nicholas P. Schmidt; Matthew E. O'Neal; Philip M. Dixon

Abstract There is increasing evidence that Aphis glycines Matsumara (Hemiptera: Aphididae) populations are negatively impacted by endemic natural enemies within North America. In Iowa, surveys of natural enemies in soybean, Glycine max (L.) Merr., conducted before the arrival of A. glycines revealed a number of species that may contribute to their mortality. We used several sampling methods to determine the diversity of the natural enemy community in Iowa soybean since the arrival of A. glycines. Natural enemies were collected using field-counts (in situ sampling), destructive counts, sweep-net sampling, and yellow-sticky cards. When predaceous arthropods were combined across all sampling methods, six orders were identified, including nine families and 13 genera. In comparison with a similar study conducted 26 yr ago, we observed fewer native coccinellids with the most abundant being the exotics Harmonia axyridis (Pallas) and Coccinella septempunctata L. (Coleoptera: Coccinellidae). Combining all foliar-based sampling methods reveals a community of four aphidophagous taxa that account for >94% of the total captured: Toxomerus spp., H. axyridis, Orius insidiosus (Say), and Chrysoperla spp. In both years, destructive counts collected fewer species with more found using field-counts, sweep-net, and yellow-sticky cards. Sweep-net and yellow-sticky cards collected more agile life-stages and species as expected from sampling methods that rely on the insects’ activity/density to be effective. Our data suggest absolute methods such as destructive and field-counts may underestimate the contribution of mobile predators on A. glycines mortality.


Journal of Economic Entomology | 2009

Impact of reduced-risk insecticides on soybean aphid and associated natural enemies.

Wayne Ohnesorg; Kevin D. Johnson; Matthew E. O'Neal

ABSTRACT Insect predators in North America suppress Aphis glycines Matsumura (Hemiptera: Aphididae) populations; however, insecticides are required when populations reach economically damaging levels. Currently, insecticides used to manage A. glycines are broad-spectrum (pyrethroids and organophosphates), and probably reduce beneficial insect abundance in soybean, Glycine max (L.) Merr. Our goal was to determine whether insecticides considered reduced-risk by the Environmental Protection Agency could protect soybean yield from A. glycines herbivory while having a limited impact on the aphids natural enemies. We compared three insecticides (imidacloprid, thiamethoxam, and pymetrozine,) to a broad-spectrum insecticide (&lgr;-cyhalothrin) and an untreated control using two application methods. We applied neonicotinoid insecticides to seeds (imidacloprid and thiamethoxam) as well as foliage (imidacloprid); pymetrozine and &lgr;-cyhalothrin were applied only to foliage. Foliage-applied insecticides had lower A. glycines populations and higher yields than the seed-applied insecticides. Among foliage-applied insecticides, pymetrozine and imidacloprid had an intermediate level of A. glycines population and yield protection compared with &lgr;-cyhalothrin and the untreated control. We monitored natural enemies with yellow sticky cards, sweep-nets, and direct observation. Before foliar insecticides were applied (i.e., before aphid populations developed) seed treatments had no observable effect on the abundance of natural enemies. After foliar insecticides were applied, differences in natural enemy abundance were observed when sampled with sweep-nets and direct observation but not with yellow sticky cards. Based on the first two sampling methods, pymetrozine and the foliage-applied imidacloprid had intermediate abundances of natural enemies compared with the untreated control and &lgr;-cyhalothrin.


Journal of Economic Entomology | 2009

Probability of Cost-Effective Management of Soybean Aphid (Hemiptera: Aphididae) in North America

Kevin D. Johnson; Matthew E. O'Neal; David W. Ragsdale; Christina DiFonzo; Scott M. Swinton; Philip M. Dixon; Bruce D. Potter; Erin W. Hodgson; Alejandro C. Costamagna

ABSTRACT Soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is one of the most damaging pests of soybean, Glycine max (L.) Merrill, in the midwestern United States and Canada. We compared three soybean aphid management techniques in three midwestern states (Iowa, Michigan, and Minnesota) for a 3-yr period (2005–2007). Management techniques included an untreated control, an insecticidal seed treatment, an insecticide fungicide tank-mix applied at flowering (i.e., a prophylactic treatment), and an integrated pest management (IPM) treatment (i.e., an insecticide applied based on a weekly scouting and an economic threshold). In 2005 and 2007, multiple locations experienced aphid population levels that exceeded the economic threshold, resulting in the application of the IPM treatment. Regardless of the timing of the application, all insecticide treatments reduced aphid populations compared with the untreated, and all treatments protected yield as compared with the untreated. Treatment efficacy and cost data were combined to compute the probability of a positive economic return. The IPM treatment had the highest probability of cost effectiveness, compared with the prophylactic tank-mix of fungicide and insecticide. The probability of surpassing the gain threshold was highest in the IPM treatment, regardless of the scouting cost assigned to the treatment (ranging from


Environmental Entomology | 2007

Alfalfa Living Mulch Advances Biological Control of Soybean Aphid

Nicholas P. Schmidt; Matthew E. O'Neal; Jeremy W. Singer

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Environmental Entomology | 2010

Constitutive and Induced Differential Accumulation of Amino Acid in Leaves of Susceptible and Resistant Soybean Plants in Response to the Soybean Aphid (Hemiptera: Aphididae)

Mariana Victoria Chiozza; Matthew E. O'Neal; Gustavo C. MacIntosh

19.76/ha). Our study further confirms that a single insecticide application can enhance the profitability of soybean production at risk of a soybean aphid outbreak if used within an IPM based system.


Journal of Integrated Pest Management | 2011

Biology of the Soybean Aphid, Aphis glycines (Hemiptera: Aphididae) in the United States

K. J. Tilmon; Erin W. Hodgson; Matthew E. O'Neal; David W. Ragsdale

Abstract Despite evidence for biological control in North America, outbreaks of the invasive soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), continue to occur on soybean (Glycine max L. Merr.). Our objectives were to determine whether natural enemies delay aphid establishment and limit subsequent population growth and whether biological control can be improved by altering the within-field habitat. We hypothesized that a living mulch would increase the abundance of the aphidophagous community in soybean and suppress A. glycines establishment and population growth. We measured natural enemy and A. glycines abundance in soybean grown with and without an alfalfa (Medicago sativa L.) living mulch. Soybean grown with an alfalfa living mulch had 45% more natural enemies and experienced a delay in A. glycines establishment that resulted in lower peak populations. From our experiments, we concluded that the current natural enemy community in Iowa can delay A. glycines establishment, and an increase in aphidophagous predator abundance lowered the rate of A. glycines population growth preventing economic populations (i.e., below the current economic threshold) from occurring. Incorporation of a living mulch had an unexpected impact on A. glycines population growth, lowering the aphids’ intrinsic rate of growth, thus providing a bottom-up suppression of A. glycines. We suggest future studies of living mulches or cover crops for A. glycines management should address both potential sources of suppression. Furthermore, our experience suggests that more consistent biological control of A. glycines may be possible with even partial resistance that slows but does not prevent reproduction.


Entomologia Experimentalis Et Applicata | 2013

Performance and prospects of Rag genes for management of soybean aphid

Louis S. Hesler; Mariana Victoria Chiozza; Matthew E. O'Neal; Gustavo C. MacIntosh; Kelley J. Tilmon; Desmi Chandrasena; Nicholas A. Tinsley; Silvia R. Cianzio; Alejandro C. Costamagna; Eileen M. Cullen; Christina DiFonzo; Bruce D. Potter; David W. Ragsdale; Kevin L. Steffey; Kenneth J. Koehler

ABSTRACT Although soybean aphid (Aphis glycines) resistance is commercially available in the form of the Rag1 gene, the mechanism of this resistance is not fully understood. Amino acids are a limiting factor for aphid growth, and there is evidence that plant amino acid composition is related to aphid resistance. Antibiotic resistance like that conferred by Rag1 could be associated in part with both protein and nonprotein free amino acids reducing survival, growth, and fecundity of the target pest. We posed two hypotheses: (1) A. glycines resistance is related to host quality in terms of free amino acids composition in the leaf, and (2) aphids may enhance host quality by inducing changes in the free amino acids composition. To test these hypotheses we conducted a field experiment using a split plot design, with soybean lines (a susceptible line and a related line carrying Rag1) as whole plots and aphid density as subplots (insecticide treated or left exposed to natural infestations). We analyzed free amino acids in leaves at three soybean developmental stages in all subplots. We observed significant whole and subplot effects on the concentration of a subset of amino acids tested. Susceptible and resistant plants had constitutive (whole-plot) differences in amino acids composition in all developmental stages analyzed. In addition, aphid-induced (subplot) responses of the plant to aphid infestation were found. We propose that the reduced nutritional quality of the resistant line and its reduced susceptibility to aphid-induced changes may contribute to aphid resistance conferred by Rag1.


Journal of Economic Entomology | 2012

Soybean Aphid (Hemiptera: Aphididae) Development on Soybean with Rag1 Alone, Rag2 Alone, and Both Genes Combined

Shaylyn Lena Wiarda; Walter R. Fehr; Matthew E. O'Neal

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is a significant insect pest of soybean in the north-central region of the United States and southern Canada, and if left untreated can reduce yield value by


Journal of Economic Entomology | 2008

Is Preventative, Concurrent Management of the Soybean Aphid (Hemiptera: Aphididae) and Bean Leaf Beetle (Coleoptera: Chrysomelidae) Possible?

Kevin D. Johnson; Matthew E. O'Neal; Jeffrey D. Bradshaw; Marlin E. Rice

2.4 billion annually. The soybean aphid is native to eastern Asia, where soybean was first domesticated, and was first detected in the United States in 2000. It quickly spread within 4 years of its discovery across 22 states and three provinces of Canada. Heavy infestations can result in a covering of sooty mold, yellow and wrinkled leaves, stunted plants, and aborted pods leading to significant yield loss of 40% or more. It can also transmit plant viruses such as Soybean mosaic virus and Alfalfa mosaic virus. The soybean aphid has a complex life cycle that involves different physical forms, sexual stages, and two host plant species-soybean and buckthorn (the overwintering host). Plant nutrition, natural enemies, climate, and weather all affect population growth rate, but the typical population doubling time is ≈6-7 days. Though at present management is primarily through broad-spectrum insecticides, biological control has a significant impact on soybean aphid population growth, and aphid-resistant soybean varieties are becoming increasingly available.

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