The Relationship Between Aphis Glycines and Soybean Mosaic Virus Incidence in Different Pest Management Systems
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The Relationship Between Aphis glycines and Soybean mosaic virus Incidence in Different Pest Management Systems M. E. Lee Burrows, USDA-ARS Plant, Soil and Nutrition Laboratory, Ithaca, NY 14853; and C. M. Boerboom and J. M. Gaska, Department of Agronomy, and C. R. Grau, Department of Plant Pathology, University of Wisconsin– Madison, Madison 53706 SMV, an economically important virus in ABSTRACT soybean (51). Glyphosate and imazamox Burrows, M. E. L., Boerboom, C. M., Gaska, J. M., and Grau, C. R. 2005. The relationship be- were selected for this study based on their tween Aphis glycines and Soybean mosaic virus incidence in different pest management systems. anticipated effect on canopy structure Plant Dis. 89:926-934. (12,17). Glyphosate applied to a gly- phosate-resistant soybean should have no The soybean aphid, Aphis glycines, causes yield loss and transmits viruses such as Soybean effect on the canopy (44), whereas ima- mosaic virus (SMV) in soybean (Glycine max). Field experiments were designed to monitor the zamox may cause chlorosis, limited necro- landing rate of A. glycines and transmission of SMV to soybean grown in six crop management sis, and shortened internodes for a limited environments. Management systems evaluated were the application of postemergence insecticide or no insecticide, and within each insecticide treatment no herbicide, glyphosate, or imazamox period of time (50). application. In 2001, early-season incidence of SMV was 2%, which increased to 80% within 18 The effect of soybean canopy closure days after the beginning of the A. glycines flight. In 2002, the incidence of SMV was 1% prior to and plant height on aphid landing rate the arrival of A. glycines, and increased to 44% within 21 days. The landing rate of A. glycines varies by aphid species (5,19). However, it was fivefold higher in 2001 than in 2002. The incidence of SMV was lower in insecticide-treated was not known whether a soybean canopy plots in 2002, but no effect of insecticide was seen in 2001. Imazamox slowed the progression of treated with insecticide and herbicides SMV incidence, but the final incidence of SMV-infected plants was the same. Glyphosate had no would alter the immigration and coloniza- consistent effect on SMV incidence. Yield was higher in the insecticide-treated plots in 2002, but tion of aphids and the frequency of subse- not 2001. Insecticide and herbicide application had no substantial effects on seed quality. quent virus transmission. The objectives of this study were to characterize the effects of insecticide and the herbicides gly- phosate and imazamox on (i) soybean The species and population dynamics of The role of A. glycines in natural epidem- canopy development, (ii) aphid landing insect pests of soybean (Glycine max (L.) ics of SMV has not been determined in rates, (iii) the seasonal progress of SMV- Merrill) have changed dramatically in the North America. Epidemiological models infected plants, and (iv) yield and seed north central region of the United States for SMV use daily alate aphid flight data quality. (15,54). The bean leaf beetle (Cerotoma to predict the incidence of SMV (31,46). trifurcata Forster) has become a prominent Because the apterous form of A. glycines MATERIALS AND METHODS pest of soybean, but the most dramatic reaches high population densities, current Agronomic protocol. AG2101, a gly- change was the introduction of the soybean epidemiological models developed for phosate-resistant soybean variety (Asgrow; aphid, Aphis glycines Matsumara. A. gly- SMV and alate aphid species may not be Monsanto, St. Louis, MO), was chosen cines was observed in Wisconsin during appropriate. because of its previous field performance the summer of 2000 and has expanded its Current SMV epidemiological models of high incidence of SMV-infected plants, range to most soybean-growing regions in were developed prior to the adoption of high foliar symptom severity, high inci- North America (1,57,60). Grain yield is glyphosate-resistant soybean varieties. Gly- dence of seed coat mottling, and reduced reduced by A. glycines by direct physiol- phosate-resistant soybean varieties have grain yield in the presence of vectors and ogic stress (38) and indirectly by transmit- been integrated with changes in soybean SMV. Plots were planted at 450,000 seeds ting Soybean mosaic virus (SMV) and management practices such as decreasing per ha on 150 Julian Date (JD), 2001, and other soybean viruses (10,22,57,60). In- row space from 0.76 to 0.18 m, reduced or 144 JD, 2002, at the West Madison Agri- tense feeding by A. glycines causes symp- no tillage, and earlier planting dates (3). cultural Research Station, Madison, WI. toms of chlorosis, rolled leaves, stunted Alteration of the canopy by herbicides, Glyphosate (Roundup Ultra, 0.84 kg plants, early maturity, defoliation, and insects, and fungal pathogens has been a.e./ha; 117 JD), metolachlor + safener sooty mold growth (Capnodium spp.) on shown to be related to yield (18,40,41). (Dual II Magnum, 2.14 kg a.i./ha; 136 JD), honeydew excreted by the aphids (58,60). Evidence thus far has not linked the applica- and metribuzin (Sencor, 0.42 kg a.i./ha; A. glycines is the first aphid species capa- tion of glyphosate to glyphosate-resistant 136 JD) were applied preplant for control ble of colonizing soybean to establish in soybean to diseases caused by fungi and of weeds in 2001. In 2002, pendimethalin North America (1,45). It is a vector of nematodes (4,7,8,27,32,36,40,49,59), but (Prowl, 1.39 kg a.i./ha) and metribuzin SMV in China (60) and has been reported the effect of glyphosate application on viral (0.42 kg a.i./ha) were incorporated into the to transmit North American isolates of diseases has not been investigated. It is soil on 135 JD prior to planting. SMV in controlled experiments (10,13,22). unknown whether soybean canopy altera- The experiment was conducted as a ran- tion due to pesticide application modifies domized complete block design with a vector activity and virus epidemiology. split-plot arrangement with four blocks. Corresponding author: Craig R. Grau Herbicides that have been shown to alter Insecticide treatment was the main plot, E-mail: [email protected] plant–virus interactions include synthetic and herbicide subplots were randomized auxins (2,4-D) (9), microtubule inhibitors within each insecticide treatment. In 2001, Accepted for publication 28 April 2005. (trifluralin) (28), and photosystem II in- the insecticide lambda-cyhalothrin (War- hibitors (metribuzin) (11). It was unknown rior 1EC, 0.02 kg a.i./ha) was applied at DOI: 10.1094/PD-89-0926 if herbicides used widely in soybean pro- growth stages V3 and R1 (184 JD and 201 © 2005 The American Phytopathological Society duction can alter the epidemiology of JD, respectively). Chlorpyrifos (Lorsban 926 Plant Disease / Vol. 89 No. 9 4E, 0.56 kg a.i./ha) was applied at R4 on canopy (30). One trap was placed in the and the rows immediately bordering the 215 JD for the control of A. glycines and center of each of 24 subplots, and height trap row were not sampled to minimize spider mites. In 2002, lambda-cyhalothrin was adjusted to within 0.5 m above the any effects of walking to the trap each day. was applied at V3 and R1 (0.02 kg a.i./ha canopy throughout the growing season. In Samples were taken in two rows on either 178 JD and 211 JD). The “no insecticide” the event of rain, irrigation, or pesticide side of the trap and bordering rows, for a treatment plots were sprayed with water. application, traps were reset after the dis- total of four rows sampled. Leaflets were The herbicides glyphosate (Roundup Ultra, turbance event. Aphids were removed from collected from the center 6 m of each sam- 0.84 kg a.e./ha) and imazamox (Raptor, the traps daily and stored in 2.0-ml flat- pling row to minimize edge effects and 0.044 kg a.e./ha) were sprayed at V3 on bottomed microcentrifuge tubes (Lab- maximize sampling intensity (2,23). Leaf- 184 JD, 2001, and 178 JD, 2002. The ima- source, Chicago, IL) in 70% ethanol until lets were sampled from rows at approxi- zamox treatment included crop oil concen- identification and enumeration. The num- mately regular, arbitrary intervals without trate (1% vol/vol) and urea ammonium ber of aphids was recorded, but only A. evaluating whether the plant was sympto- nitrate (4.7 liters/ha of 28-0-0) as adju- glycines was identified to species. A. gly- matic. Samples were chilled on ice, stored vants. The no herbicide control plots were cines was identified by key traits that sepa- at 4°C, and individual leaflets extracted not sprayed. rate them from closely related species (55). using a leaf press (Ravenel Specialties Rows were 75 cm wide, and 3-m-wide Voucher specimens of A. glycines from Corp., Seneca, SC) and 1 ml of phosphate alleys were cut between main plot insecti- this study have been deposited in the Uni- buffered saline (0.15 M PBS, pH 7.2; Ag- cide treatments for ease of spraying. No versity of Wisconsin Department of Ento- dia, Inc., Elkhart, IN). Sap was placed in alleys were cut between herbicide sub- mology Insect Research Collection, Madi- 1.5-ml polypropylene microcentrifuge tubes plots. Subplots were 9.1 m wide by 12.2 m son. (Labsource), frozen at –20°C for storage, long in 2001 and 18.3 m wide by 13.7 m Colonization by A. glycines was moni- and assayed using a biotin-avidin double- long in 2002. In 2002, the field was irri- tored following its initial appearance.