Spatial distribution of Aphis glycines (Hemiptera: Aphididae): a summary of the suction trap network.

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is an economically important pest of soybean, Glycine max (L.) Merrill, in the United States. Phenological information of A. glycines is limited; specifically, little is known about factors guiding migrating aphids and potential impacts of long distance flights on local population dynamics. Increasing our understanding of A. glycines population dynamics may improve predictions of A. glycines outbreaks and improve management efforts. In 2005 a suction trap network was established in seven Midwest states to monitor the occurrence of alates. By 2006, this network expanded to 10 states and consisted of 42 traps. The goal of the STN was to monitor movement of A. glycines from their overwintering host Rhamnus spp. to soybean in spring, movement among soybean fields during summer, and emigration from soybean to Rhamnus in fall. The objective of this study was to infer movement patterns of A. glycines on a regional scale based on trap captures, and determine the suitability of certain statistical methods for future analyses. Overall, alates were not commonly collected in suction traps until June. The most alates were collected during a 3-wk period in the summer (late July to mid-August), followed by the fall, with a peak capture period during the last 2 wk of September. Alate captures were positively correlated with latitude, a pattern consistent with the distribution of Rhamnus in the United States, suggesting that more southern regions are infested by immigrants from the north.

Ecology and management of the soybean aphid in North America.

The soybean aphid, Aphis glycines Matsumura, has become the single most important arthropod pest of soybeans in North America. Native to Asia, this invasive species was first discovered in North America in July 2000 and has rapidly spread throughout the northcentral United States, much of southeastern Canada, and the northeastern United States. In response, important elements of the ecology of the soybean aphid in North America have been elucidated, with economic thresholds, sampling plans, and chemical control recommendations widely adopted. Aphid-resistant soybean varieties were available to growers in 2010. The preexisting community of aphid natural enemies has been highly effective in suppressing aphid populations in many situations, and classical biological control efforts have focused on the addition of parasitoids of Asian origin. The keys to sustainable management of this pest include understanding linkages between the soybean aphid and other introduced and native species in a landscape context along with continued development of aphid-resistant varieties.

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.

Non-target impacts of soybean rust fungicides on the fungal entomopathogens of soybean aphid.

Soybean aphid, Aphis glycines, has caused serious economic damage to soybean across the North Central US since its introduction to North America in 2000. The management of another invasive soybean pest, Asian soybean rust, Phakopsora pachyrhizi, using foliar fungicide applications has the potential to impact soybean aphid populations by suppressing beneficial fungal entomopathogens. In 2005 and 2006, we applied recommended soybean rust fungicide treatments, consisting of strobilurin and triazole fungicides, to small soybean plots in two locations to assess if such applications might suppress aphid fungal epizootics. In Lamberton, MN, in 2005, during the epizootic, fungicide-treated plots averaged 2.0+/-0.7% (mean+/-SE) disease prevalence while untreated plots averaged 14.2+/-5.6%. In 2007, we applied strobilurin and strobilurin-triazole mix fungicides to single-plant microplots either before or after release of Pandora neoaphidis, the most commonly observed aphid pathogen in 2005 and 2006. Treatments that contained a mixture of two active ingredients significantly lowered peak and cumulative aphid disease prevalence in both early and late reproductive stage soybeans indicating that fungicide mixtures used to manage soybean rust can negatively impact an aphid-specific fungal pathogen. However, no consistent soybean aphid population response was observed in these studies of low levels of aphid fungal infection.

Development and validation of node-based sample units for estimating soybean aphid (Hemiptera: Aphididae) densities in field cage experiments.

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is currently the most important insect threat to soybean, Clycine max (L.) Merr., production in the North Central United States. Field cage studies are a key tool in investigating the potential of natural enemies and host plant resistance to control this pest. However, a major constraint in the use of cage studies is the limited number of treatments and replicates that can be used as aphid densities frequently become so large as to limit the number of experimental units that can be quantified. One way to overcome this limitation is to develop methods that estimate whole-plant aphid densities based on a reduced sampling plan. Here, we extend an existing method, node-sampling, used for estimating aphid populations in open field conditions and apply it to caged populations. We show that parameters calculated under open field conditions are inappropriate to estimate caged populations. In contrast, using four independent data sets of caged populations and a cross-validation technique, we demonstrate that a three-node sampling unit and a weighted formula provide accurate and robust estimates of whole-plant aphid density. This method reduced the number of aphids counted per plant by and average of 60%, with greater reductions at higher aphid densities. We further demonstrate that nearly identical statistical results were obtained when whole-plant or node-sampling estimates were used in the analysis of two case studies. The reduced sample unit method developed here saves time without sacrificing efficiency so that more plants, replications, or studies can be conducted that will lead to improved soybean aphid management.

Probability of cost-effective management of soybean aphid (Hemiptera: Aphididae) in North America.

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 $0.00 to $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.

Within-plant bottom-up effects mediate non-consumptive impacts of top-down control of soybean aphids.

There is increasing evidence that top-down controls have strong non-consumptive effects on herbivore populations. However, little is known about how these non-consumptive effects relate to bottom-up influences. Using a series of field trials, we tested how changes in top-down and bottom-up controls at the within-plant scale interact to increase herbivore suppression. In the first experiment, we manipulated access of natural populations of predators (primarily lady beetles) to controlled numbers of A. glycines on upper (i.e. vigorous-growing) versus lower (i.e. slow-growing) soybean nodes and under contrasting plant ages. In a second experiment, we measured aphid dispersion in response to predation. Bottom-up and top-down controls had additive effects on A. glycines population growth. Plant age and within-plant quality had significant bottom-up effects on aphid size and population growth. However, top-down control was the dominant force suppressing aphid population growth, and completely counteracted bottom-up effects at the plant and within-plant scales. The intensity of predation was higher on upper than lower soybean nodes, and resulted in a non-consumptive reduction in aphid population growth because most of the surviving aphids were located on lower plant nodes, where rates of increase were reduced. No effects of predation on aphid dispersal among plants were detected, suggesting an absence of predator avoidance behavior by A. glycines. Our results revealed significant non-consumptive predator impacts on aphids due to the asymmetric intensity of predation at the within-plant scale, suggesting that low numbers of predators are highly effective at suppressing aphid populations.

Environmental consequences of invasive species: greenhouse gas emissions of insecticide use and the role of biological control in reducing emissions.

Greenhouse gas emissions associated with pesticide applications against invasive species constitute an environmental cost of species invasions that has remained largely unrecognized. Here we calculate greenhouse gas emissions associated with the invasion of an agricultural pest from Asia to North America. The soybean aphid, Aphis glycines, was first discovered in North America in 2000, and has led to a substantial increase in insecticide use in soybeans. We estimate that the manufacture, transport, and application of insecticides against soybean aphid results in approximately 10.6 kg of carbon dioxide (CO2) equivalent greenhouse gasses being emitted per hectare of soybeans treated. Given the acreage sprayed, this has led to annual emissions of between 6 and 40 million kg of CO2 equivalent greenhouse gasses in the United States since the invasion of soybean aphid, depending on pest population size. Emissions would be higher were it not for the development of a threshold aphid density below which farmers are advised not to spray. Without a threshold, farmers tend to spray preemptively and the threshold allows farmers to take advantage of naturally occurring biological control of the soybean aphid, which can be substantial. We find that adoption of the soybean aphid economic threshold can lead to emission reductions of approximately 300 million kg of CO2 equivalent greenhouse gases per year in the United States. Previous studies have documented that biological control agents such as lady beetles are capable of suppressing aphid densities below this threshold in over half of the soybean acreage in the U.S. Given the acreages involved this suggests that biological control results in annual emission reductions of over 200 million kg of CO2 equivalents. These analyses show how interactions between invasive species and organisms that suppress them can interact to affect greenhouse gas emissions.

Novel and viable acetylcholinesterase target site for developing effective and environmentally safe insecticides.

Insect pests are responsible for human suffering and financial losses worldwide. New and environmentally safe insecticides are urgently needed to cope with these serious problems. Resistance to current insecticides has resulted in a resurgence of insect pests, and growing concerns about insecticide toxicity to humans discourage the use of insecticides for pest control. The small market for insecticides has hampered insecticide development; however, advances in genomics and structural genomics offer new opportunities to develop insecticides that are less dependent on the insecticide market. This review summarizes the literature data that support the hypothesis that an insect-specific cysteine residue located at the opening of the acetylcholinesterase active site is a promising target site for developing new insecticides with reduced off-target toxicity and low propensity for insect resistance. These data are used to discuss the differences between targeting the insect-specific cysteine residue and targeting the ubiquitous catalytic serine residue of acetylcholinesterase from the perspective of reducing off-target toxicity and insect resistance. Also discussed is the prospect of developing cysteine-targeting anticholinesterases as effective and environmentally safe insecticides for control of disease vectors, crop damage, and residential insect pests within the financial confines of the present insecticide market.

Insect-specific irreversible inhibitors of acetylcholinesterase in pests including the bed bug, the eastern yellowjacket, German and American cockroaches, and the confused flour beetle.

Insecticides directed against acetylcholinesterase (AChE) are facing increased resistance among target species as well as increasing concerns for human toxicity. The result has been a resurgence of disease vectors, insects destructive to agriculture, and residential pests. We previously reported a free cysteine (Cys) residue at the entrance to the AChE active site in some insects but not higher vertebrates. We also reported Cys-targeting methanethiosulfonate molecules (AMTSn), which, under conditions that spared human AChE, caused total irreversible inhibition of aphid AChE, 95% inhibition of AChE from the malaria vector mosquito (Anopheles gambia), and >80% inhibition of activity from the yellow fever mosquito (Aedes aegypti) and northern house mosquito (Culex pipiens). We now find the same compounds inhibit AChE from cockroaches (Blattella germanica and Periplaneta americana), the flour beetle (Tribolium confusum), the multi-colored Asian ladybird beetle (Harmonia axyridis), the bed bug (Cimex lectularius), and a wasp (Vespula maculifrons), with IC(50) values of approximately 1-11muM. Our results support further study of Cys-targeting inhibitors as conceptually novel insecticides that may be free of resistance in a range of insect pests and disease vectors and, compared with current compounds, should demonstrate much lower toxicity to mammals, birds, and fish.

Selective and irreversible inhibitors of mosquito acetylcholinesterases for controlling malaria and other mosquito-borne diseases.

New insecticides are urgently needed because resistance to current insecticides allows resurgence of disease-transmitting mosquitoes while concerns for human toxicity from current compounds are growing. We previously reported the finding of a free cysteine (Cys) residue at the entrance of the active site of acetylcholinesterase (AChE) in some insects but not in mammals, birds, and fish. These insects have two AChE genes (AP and AO), and only AP-AChE carries the Cys residue. Most of these insects are disease vectors such as the African malaria mosquito (Anopheles gambiae sensu stricto) or crop pests such as aphids. Recently we reported a Cys-targeting small molecule that irreversibly inhibited all AChE activity extracted from aphids while an identical exposure caused no effect on the human AChE. Full inhibition of AChE in aphids indicates that AP-AChE contributes most of the enzymatic activity and suggests that the Cys residue might serve as a target for developing better aphicides. It is therefore worth investigating whether the Cys-targeting strategy is applicable to mosquitocides. Herein, we report that, under conditions that spare the human AChE, a methanethiosulfonate-containing molecule at 6 microM irreversibly inhibited 95% of the AChE activity extracted from An. gambiae s. str. and >80% of the activity from the yellow fever mosquito (Aedes aegypti L.) or the northern house mosquito (Culex pipiens L.) that is a vector of St. Louis encephalitis. This type of inhibition is fast ( approximately 30 min) and due to conjugation of the inhibitor to the active-site Cys of mosquito AP-AChE, according to our observed reactivation of the methanethiosulfonate-inhibited AChE by 2-mercaptoethanol. We also note that our sulfhydryl agents partially and irreversibly inhibited the human AChE after prolonged exposure (>4 hr). This slow inhibition is due to partial enzyme denaturation by the inhibitor and/or micelles of the inhibitor, according to our studies using atomic force microscopy, circular dichroism spectroscopy, X-ray crystallography, time-resolved fluorescence spectroscopy, and liquid chromatography triple quadrupole mass spectrometry. These results support our view that the mosquito-specific Cys is a viable target for developing new mosquitocides to control disease vectors and to alleviate resistance problems with reduced toxicity toward non-target species.