Biology and Economics of Recommendations for Insecticide-Based Management of Soybean Aphid

Soybean aphid, Aphis glycines Matsumura, remains the key insect pest of soybean, Glycine max (L.) Merrill, in the north-central United States. Management of this pest has relied primarily on scouting and application of foliar insecticides based on an economic threshold (ET) of 250 aphids per plant. This review explains why this ET remains valid for soybean aphid management, despite changes in crop value and input costs. In particular, we review how soybean aphid impacts soybean yield, the role of biology and economics in recommendations for soybean aphid management, and the shortand long-term consequences of inappropriately timed insecticide applications. Introduction The soybean aphid, Aphis glycines Matsumura (Fig. 1), was first detected in the United States in 2000. Prior to the invasion by this pest, insecticide applications to soybean, Glycine max (L.) Merrill, in the north-central United States were rare (USDANASS 1999), but during the last region-wide outbreak in 2005, millions of acres were treated for soybean aphid (USDA-NASS 2005). Although outbreaks are less common in some states since the mid-2000s (Bahlai et al. 2015), soybean aphid is still the key insect pest of soybean in this region (Hurley and Mitchell 2014). In North America, a tremendous amount of research and observational data have been generated on soybean aphid since its initial detection, and tools and knowledge now exist for effective management of this pest (Hodgson et al. 2012; Ragsdale et al. 2004; Ragsdale et al. 2011; Tilmon et al. 2011). Published in Plant Health Progress 17 (2016), pp 265-269. doi:10.1094/PHP-RV-16-0061 Copyright © 2016 The American Phytopathological Society. Used by permission. Accepted for publication December 13, 2016. Biology and Economics of Recommendations for Insecticide-Based Management of Soybean Aphid Robert L. Koch, Department of Entomology, University of Minnesota, Saint Paul 55108 Bruce D. Potter, Southwest Research and Outreach Center, University of Minnesota, Lamberton 56152 Phillip A. Glogoza, University of Minnesota Extension, Moorhead 56560 Erin W. Hodgson, Department of Entomology, Iowa State University, Ames 50011 Christian H. Krupke, Department of Entomology, Purdue University, West Lafayette, IN 47907 John F. Tooker, Department of Entomology, Penn State University, University Park 16802 Christina D. DiFonzo, Department of Entomology, Michigan State University, East Lansing 48824 Andrew P. Michel and Kelley J. Tilmon, Department of Entomology, The Ohio State University, Wooster 44691 Travis J. Prochaska, North Central Research Extension Center, North Dakota State University Extension, Minot 58701 Janet J. Knodel, Department of Plant Pathology, North Dakota State University, Fargo 58102 Robert J. Wright, Department of Entomology, University of Nebraska-Lincoln 68583 Thomas E. Hunt, Department of Entomology, University of Nebraska-Lincoln, Concord 68728 Bryan Jensen, Integrated Pest Management, University of Wisconsin, Madison 53706 Adam J. Varenhorst, Agronomy, Horticulture, and Plant Science Department, South Dakota State University, Brookings 57006 Brian P. McCornack, Department of Entomology, Kansas State University, Manhattan 66506 Kelly A. Estes and Joseph L. Spencer, Illinois Natural History Survey, University of Illinois, Champaign 61820 Corresponding author — Robert L. Koch. Email: [email protected] 265 digitalcommons.unl.edu Figure 1. Soybean aphid colony on soybean (photo by A. Varenhorst). 266 Koch et al . in Plant Health Progress 17 (2016) Soybean aphid management recommendations, including the economic threshold (Ragsdale et al. 2007), developed by landgrant universities are based on replicated research evaluated by other agricultural scientists (i.e., peer-reviewed) before publication and dissemination. These recommendations take into consideration pest biology, as well as effectiveness and shortand long-term economic and environmental implications of management tactics. Economic conditions (e.g., crop and input prices) have changed since publication of soybean aphid management recommendations (Ragsdale et al. 2007; Tilmon et al. 2011). Here, we present a research-based review updating what is known about soybean aphid, including the potential effects on yield and cost-effective management for this pest. Soybean Aphid Injury to Soybean All aphids, including soybean aphid, feed on plant fluids by inserting piercing-sucking mouthparts directly into the phloem and removing water and nutrients (Pettersson et al. 2007), which can decrease photosynthetic rates of soybean (Macedo et al. 2003). To survive and reproduce, soybean aphids require specific nitrogen-rich amino acids that are present in plant fluids at low concentrations (Douglas and van Emden 2007; Mittler and Douglas 2003; Walter and DiFonzo 2007), which means they must ingest large quantities of plant fluids to fulfill their nutritional needs (Douglas and van Emden 2007). Nutrient (Myers et al. 2005; Myers and Gratton 2006; Walter and DiFonzo 2007) and moisture (Nachappa et al. 2016) status of soybean influences the composition of the plant fluids and, in turn, soybean aphid. In addition, quality of plant fluids likely influences location of soybean aphids within the canopy as plants age (McCornack et al. 2008). Excess water and sugars from the plant fluids are excreted by aphids as sticky waste (Malumphy 1997) called “honeydew,” which accumulates on leaves of heavily infested plants. Sooty mold fungus (Fig. 2) can grow on honeydew-covered leaves, blocking sunlight and further interfering with photosynthesis (Malumphy 1997; Lemos Filho and Paiva 2006). Feeding by soybean aphid on soybean can reduce plant growth, pod number, seed number, seed weight, and seed oil concentration (Beckendorf et al. 2008; Ragsdale et al. 2011). Prolonged infestations beginning early in the season can affect all soybean yield components, while later infestations tend to only reduce seed size (Beckendorf et al. 2008). Soybean aphid feeding can also facilitate population growth of soybean cyst nematode, Heterodera glycines Ichinhoe (McCarville et al. 2014), and transmit several disease-causing viruses of soybean (e.g., Soybean mosaic virus and Alfalfa mosaic virus) (Hill et al. 2001; Mueller and Grau 2007) and other crops (Davis et al. 2005; Davis and Radcliffe 2008; DiFonzo and Agle 2008; Wang et al. 2006). Because these soybean viruses are not currently recognized as consistent, significant threats to yield in the north-central United States, they are not accounted for in general soybean aphid management recommendations. Soybean aphids are not known to transmit fungal or bacterial diseases to soybean. However, soybean aphid and some pathogens may co-occur at similar times or be favored by similar environmental conditions, which may result in the incorrect assumption that a disease was transmitted by aphids or the pathogen entered the plant through feeding wounds caused by aphids. In reality, compared to defoliating insects, aphid feeding creates minimal wounding; plant cells along the feeding tracks generally are not damaged (Dixon 1998). Yield loss from soybean aphid is a function of the number of aphids on the plant and the duration of their feeding (Ragsdale et al. 2007). With these two parameters, aphid population pressure over time can be calculated as cumulative aphid-days (Hanafi et al. 1989). For example, the population pressure of a single soybean aphid on a plant for 10 days is equal to 10 aphid-days (1 aphid × 10 days), while that of 200 aphids on a plant for 20 days is equal to 4,000 aphid-days (200 aphids × 20 days). The aphidday concept has proven to be a consistent indicator of how soybean yield responds to aphid populations (Ragsdale et al. 2007) and has been utilized for aphids in other crops (Kieckhefer et al. 1995). Biological and Economic Considerations in Soybean Aphid Management Reliable treatment decisions for soybean aphid start with field estimates of aphid densities (i.e., numbers of aphids per plant) (Hodgson et al. 2004). Soybean fields should be scouted on a regular basis because soybean aphid populations can increase rapidly (Hodgson et al. 2012; McCornack et al. 2004; Ragsdale et al. 2007), particularly when winged aphids migrate within and between fields (Costamagna et al. 2013). Early-season (i.e., May through mid-July) scouting should focus on fields that have histories of early colonization by soybean aphids, particularly early-planted fields and fields near buckthorn, Rhamnus spp., the overwintering host of soybean aphid (Bahlai et al. 2010). More fields should be scouted as soybean aphid populations develop throughout the growing season and plants begin to enter reproductive (R) stages. There may not be a need to visit every field every week, but enough fields should be checked to detect increasing aphid populations that require weekly sampling. NCSRP (2013) and Extension bulletins provide more detailed recommendations for scouting. Treatment decisions for soybean aphid are based on the relationship between aphid pressure and damage. The lowest pest population that causes measurable yield loss is called the damage boundary, shown on a generalized damage curve in Figure 3. The damage boundary is a function of the interaction of the pest, crop, and environment and is independent of changing economic factors such as crop value and input costs (Pedigo Figure 2. A clean soybean leaf (bottom) compared to a leaf from an aphidinfested plant (top) which is covered with honeydew and sooty mold (photo by B. McCornack). Insect ic ide-Based Management of Soybean Aphid 267 et al. 1986). No quantifiable yield loss occurs while pest pressure remains below the damage boundary. For soybean aphid, the damage boundary is estimated at about 4,000 to 5,000 cumulative aphid-days (Ragsdale et al. 2007; Tilmon 2014). When the data for the yield-loss relationship for soybean as a function of aphid pressure (Ragsdale et al. 2007) are regressed over a range of 0 to 5,000 cumulative aphid-days no yield loss is detected with increasing aphid pressure (y = −0.000005x + 1.0074, r2 = 0.025, where x is cumulative aphid-days and y is proportion maximum yield). Further along the damage curve (Fig. 3) is the economic injury level (EIL), which is the point at which the yield loss from insect injury is equal to the cost of a management action, such as an insecticide application (Pedigo et al. 1986). At the EIL, an insecticide application is economically justified. The EIL considers the yield-loss relationship for the pest and crop, treatment costs and efficacy, and expected crop yields and value (Pedigo et al. 1986). In the case of soybean aphid on soybean, the EIL is approximately 5,500 cumulative aphid-days (Ragsdale et al. 2007). To prevent a pest population from reaching the EIL, a triggerpoint or economic threshold (ET) is set to take action at a lower pest density (Pedigo et al. 1986). The ET can also be referred to as an action threshold or treatment threshold. For most insect pests the ET is set well below the EIL to minimize the chance of incurring economic loss. To more readily apply the aphid-yield loss relationship to field scouting and aphid management decisions, a value in terms of aphids per plant was calculated for use as the ET to apply an insecticide and to reduce the likelihood of a population reaching an EIL. For soybean through the R5 growth stage (Fehr and Caviness 1977), an ET of 250 soybean aphids per plant with more than 80% of plants infested and aphid populations increasing was established to prevent soybean aphid populations from reaching the EIL (see above), which has been calculated to occur at about 675 aphids per plant (Ragsdale et al. 2007). In fact, the ET for soybean aphid is also lower than the damage boundary (see above), which has been estimated to occur at 485 to 600 aphids per plant (Tilmon 2014). To determine the values for the damage boundary, EIL and ET for soybean aphid, thousands of whole-plant aphid counts were taken at frequent intervals throughout the growing season, replicated over multiple years, and at multiple locations in multiple states (Ragsdale et al. 2007). The importance of factors other than pest abundance on relationships between pest populations and crop yields has been acknowledged (Pedigo et al. 1986). Such factors are implicitly incorporated into the ET for soybean aphid, because the large dataset used for its development incorporated a wide range of soybean growing environments, along with variation in plant growth stage, natural enemy abundance, moisture, and other stresses. Attempts have been made to explicitly account for variability in some of these factors for soybean aphid management; however, such dynamic thresholds are currently not recommended for soybean aphid management in the north-central United States. Catangui et al. (2009) developed EILs for soybean aphid on different soybean growth stages; however, the caged conditions under which their experiment was performed affected environment, biological control and aphid emigration, and limit the ability to implement their recommendations for soybean aphid management (O’Neal et al. 2010). ETs accounting for natural enemy abundance have also been developed (Hallet et al. 2014; Zhang and Swinton 2009; Zhang and Swinton 2012), but have not been adequately validated for implementation in the north-central United States. Further research to develop and validate such recommendations is encouraged. In the decade since the establishment of ET for soybean aphid (Ragsdale et al. 2007), university-based research has continued to reconfirm the ET and damage boundary values for soybean aphid (Hodgson and VanNostrand 2014, 2015, 2016; Johnson et al. 2009). Although the EIL may vary based on changing value of soybean or insecticide costs, no consistent economic gain can be found with a reduced ET for soybean aphid. This is because the ET of 250 aphids per plant is already set well below the damage boundary, so no measurable yield loss occurs at this soybean aphid population level. Costs Associated With Treating Soybean Aphids Too Early The ET for soybean aphid is best viewed as a fixed action or treatment threshold. In the case of soybean aphid, using a higher ET reduces the lead-time for insecticide applications and increases risk of exceeding the EIL from rapidly increasing aphid populations. In contrast, using a lower ET may provide more lead-time for insecticide applications, but curtails the opportunity for natural enemies and environmental conditions to suppress soybean aphid populations. In addition, lowering the ET also has the potential to result in wasted insecticide applications, by treating fields that will never approach the EIL. Unlike the longestablished 250-aphid benchmark, both higher and lower ET’s have not been adequately validated in field settings. Therefore, a sliding scale for the ET currently cannot be recommended for soybean aphid management. While some newer insecticides target a narrower range of insects (Knodel et al. 2016; Tran et al. 2016; Varenhorst and O’Neal Figure 3. Damage curve showing a generalized relationship between pest population and crop yield (modified from Pedigo et al. 1986). 268 Koch et al . in Plant Health Progress 17 (2016) 2012), most insecticides used for soybean aphid management in the north-central United States are broad-spectrum organophosphates and pyrethroids (Hodgson et al. 2012; Olson et al. 2008). These non-specific insecticides not only kill aphids, but also kill beneficial insects (e.g., lady beetles, minute pirate bugs, parasitic wasps) that naturally suppress soybean aphid populations. In the absence of these beneficial insects soybean aphid populations may rebound, sometimes increasing to levels greater than before treatment. The cost of an additional insecticide application to control a rebounding soybean aphid population further narrows profit margins. By using the ET to make management decisions, a robust suite of beneficial insects has a chance to suppress soybean aphid populations and possibly prevent aphids from reaching the EIL. Protection offered by early applications of insecticides may be overestimated. After application, insecticide residues will kill insects for varying lengths of time, but often only a few days and insecticide activity declines over time. Most insecticides registered for soybean aphid management are not systemic, so soybean foliage emerging after the insecticide application is not protected from immigrating aphids. Foliar applications of systemic insecticides, such as neonicotinoids, are absorbed by plants and typically move (i.e., translocated) upward to a limited extent within the plants (Buchholz and Nauen 2002; Nauen et al. 1999; Weichel and Nauen 2003). However, this translocation of insecticide to unsprayed foliage may be insufficient to suppress pest populations (Derksen et al. 2015). Early treatment reduces or eliminates the cost efficiencies of a single, well-timed threshold-based treatment (Johnson et al. 2009). Furthermore, there are additional long-term costs of spraying too early or too often. For example, insecticide resistance has developed in other aphid species (Foster et al. 2007) and was documented in soybean aphid in Asia (Wang et al. 2011). More concerning, field-level failures of pyrethroid insecticides against soybean aphid were recently reported in Minnesota (Koch and Potter 2016). Conclusions To minimize the risk of an unnecessary insecticide application, it is important to consider the messenger and source of information related to pest management recommendations. The recommendations reviewed here are based on replicated, peer-reviewed research and successfully implemented over millions of acres for more than a decade. Changing economics may affect the EIL for soybean aphid, but it is prudent to remember that the ET of 250 aphids per plant is conservative and remains valid, because this value is far lower than the damage boundary. Although many generic insecticides are touted as inexpensive insurance compared to other inputs, they do not consistently provide a return on investment when used prophylactically. In large farming operations, a few dollars per acre for an additional input can add up quickly. Preemptive, insurance-type insecticide applications made at very low aphid densities carry well-documented pitfalls, including development of insecticide resistance and outbreaks of secondary pests such as spider mites. Furthermore, tank mixing an insecticide with an herbicide, fungicide, or liquid fertilizer application may result in reduced effectiveness, because the optimum timing or method of application for the tank-mix partners may differ. 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