JUST THE FACTS:

A review of the biology and economics behind soybean aphid insecticide recommendations University of Minnesota: Bruce Po er, Robert Koch & Phillip Glogoza; Iowa State University: Erin Hodgson; Purdue University: Chris an Krupke; Penn State University: John Tooker; Michigan State University: Chris DiFonzo ; Ohio State University: Andrew Michel & Kelley Tilmon; North Dakota State University: Travis Prochaska & Janet Knodel; University of Nebraska: Robert Wright & Thomas E. Hunt; University of Wisconsin: Bryan Jensen; University of Illinois: Kelley Estes & Joseph Spencer

Before soybean aphid was iden fied as a pest of soybean in the U.S. in 2000, insec cide applica ons to northern soybean crops were rare, targe ng sporadic insect and mite outbreaks. Although large infesta ons have been rela vely uncommon since the early to mid‐2000’s, the soybean aphid is unques onably s ll the key insect pest of soybeans in many North Central states. A tremendous amount of research and observa onal data has been obtained for this pest since its introduc on and we have the tools and the knowledge to manage this pest effec vely. The ques on is where to get the best informa on? There is a wide array of pest management advice and informa on available for soybean producers. The internet is par cularly rife with newsle ers, social media pos ngs, and videos that all purport to give expert advice. It’s wise to always consider the source of the informa on and also evaluate what it is actually based on ‐ making a statement with absolute certainty doesn’t necessarily make it a fact. As scien sts at universi es, we make pest management recommenda ons that are based on repeated and controlled studies, sta s cal tests and, ul mately, a system called “peer review” that ensures that what we publish is ve ed thoroughly and evaluated by other scien sts, o en anonymously. However, for many of the sources of informa on available to soybean farmers, there is no review of any kind. As a result, many of the “recommenda ons” from en es not relying on sound science are never challenged or cri cally evaluated. As such, they are just opinions. The Land‐Grant University system and the Extension mission were created to conduct unbiased research and provide educa on for the public good. The soybean aphid management recommenda ons from Land‐Grant Universi es are based on replicated research that is evaluated by other agricultural researchers and educators (peer‐reviewed) before it is published and disseminated. These recommenda ons aren’t just anecdotal, or based on hunches and feelings. They’re based on facts, established crop and pest biology, effec veness of single or combined management tac cs, short‐ and long‐term economic costs and environmental implica ons. As farmers and their advisors begin to find soybean aphids in their fields, the ming is right for a fact‐based review of what is known about soybean aphid, their effect on yield, and cost‐effec ve management of this pest.

HOW CAN SOYBEAN APHIDS REDUCE SOYBEAN YIELD? The soybean aphid feeds on the phloem fluids (some mes referred to as "sap") by inser ng piercing‐sucking mouthparts directly into the phloem vessels that carry products of photosynthesis from the leaves to other parts of the plant. Prior to feeding, aphids "taste" the sap to determine if the plant is a suitable host species and if the quality is acceptable. Once they se le and begin feeding, the injury from soybean aphid infesta ons can reduce plant growth, Early‐season soybean aphid pod number, seed number, seed weight and seed oil concentra on (2, infesta on being fed upon by a lady beetle. 24). Early and prolonged aphid infesta ons can affect all yield components, while later infesta ons tend to only reduce seed size (2). In addi on, soybean aphids decrease photosynthesis rates of soybean plants (11). Direct yield loss from soybean aphid feeding does not occur when the first (or five or ten) aphids begin feeding. Today's soybean varie es are equipped to handle minor challenges, including a few aphids. Yield loss from soybean aphid is related to how many soybean aphids are present and for how long the aphids are present and feeding. The amount of aphid popula on pressure over me is calculated as aphid‐days. Simply put, this is the average number of aphids on a plant mul plied by the number of days they are present. A single soybean aphid on a plant for 10 days is equal to 10 aphid‐days, 200 aphids on a plant for 20 days is equal to 4,000 aphid‐days, and so on. This aphid‐day concept proved to be a good indicator of how soybean yield responded to aphid popula ons (23). Feeding by aphids does not cause the plant to 'leak sap'. Soybean aphids require specific nitrogen‐rich amino acids that are present in plant fluids at low concentra ons (16, 25). Therefore, aphids must consume large volumes of sap to acquire enough nutri on. Excess water and sugars from the sap are excreted by the aphids as waste. This is called honeydew. It is the s cky, shiny substance that accumulates on leaves of aphid‐infested plants. The sugary honeydew is some mes fed on and used by other insects as an energy source. A fungus called sooty mold also u lizes aphid honeydew and results in a dark coa ng on soybean leaves which, may block sunlight and interfere with photosynthesis (12, 10, 8).

Soybean aphids are not known to transmit fungal or bacterial diseases to soybean. Because soybean aphids and soybean pathogens are associated with certain environments, some people may wrongly assume that the presence of a fungal disease (such as charcoal rot) means that the disease was transmi ed by aphids or that the disease entered through the wounds caused by aphids. However, aphid feeding can transmit disease‐causing viruses from one plant to another. The soybean aphid has been associated with the transmission of several viral diseases of soybean, such as soybean mosaic virus (6), alfalfa mosaic virus (17), and others (26). Because these viral diseases are not currently considered significant threats to soybean yield in the North Central region, they are not directly accounted for in general aphid management recommenda ons. The “tas ng” or probing of plants by soybean aphids can also transmit viruses in plants that are not soybean aphid hosts, such as dry beans (18) and potato (3, 4). This effect in other crops is par cularly pronounced when soybean aphid popula ons are high.

ECONOMICS OF SOYBEAN APHID INFESTATIONS: MATH AND BIOLOGY MATTER The lowest level of aphid infesta on that has been shown to cause yield loss in soybean is several thousand aphid‐days. This value, referred to as the damage boundary, is a biological rela onship between the insect, crop, and environment, and is independent of crop and input costs. Below the damage boundary, no damage can be measured. Therefore, management efforts directed at trea ng aphid levels well below the damage boundary cannot provide a return on investment. Rela onship of insect popula on and crop yield (Modified from Pedigo et al. 1986).

referred to as an ac on threshold or treatment threshold. In most thresholds for insect pests, including soybean aphid, the ET occurs well before the EIL to minimize the chance of the grower incurring economic loss. In fact, the ET for soybean aphid occurs before the damage boundary. In addi on to costs, the ET may take into account factors like insec cide effec veness, rate of insect reproduc on, crop development, and lead‐ mes for insec cide applica on. All of the values and statements above are based on data. To determine the values for damage boundary, EIL and ET for soybean aphid, thousands of whole‐plant aphid counts were taken at frequent intervals through the growing season. Furthermore, the large mul ‐state data set that went into these calcula ons included a wide range of soybean growing environments, including moisture varia on and other stresses. The economic threshold of 250 soybean aphids per plant, more than 80% of plants infested and aphid popula ons increasing (23) was established to prevent popula ons from reaching the EIL. These values were determined by closely monitoring aphid popula ons in research plots. It has been nearly a decade since the current threshold was developed and published, and University research con nues to support these values. However, some people have ques oned the con nued validity of original soybean aphid ET of 250 aphids per plant, which was calculated including economic condi ons from the mid‐2000s. Calcula ons performed using current economic condi ons (which are different now), but without regard to biology (which has not changed), may suggest that a lower ET should be used for aphid management. This is based on faulty logic. Aphid biology and how the plant reacts to aphids make the exercise meaningless. No significant gain can be found at those lower aphid numbers (remember the ET of 250 aphids per plant is already well below the damage boundary), AND low numbers of aphids o en don’t reach the EIL. The soybean aphid ET is best viewed as a fixed ac on or treatment threshold, unlike some, more flexible thresholds for other pests. In the case of soybean aphid, raising the threshold reduces lead‐ me for applica ons and increases risk of economic loss from rapidly increasing aphid popula ons. Lowering the threshold may provide a bit more lead‐ me for insec cide applica on, but it also reduces the chances for natural enemies and the some mes‐harsh environment of a soybean field to solve the problem for you. Lowering the threshold reduces your ability to treat only those fields facing a reasonably high risk for yield loss. Therefore, a sliding scale that lowers the ET is not recommended.

The economic injury level (EIL) is the point at which the yield loss from insect damage is equal to the cost of a management ac on, such as an insec cide applica on. Insec cide applica ons made to pest popula ons that have not reached this point, and are unlikely to reach it, would not provide any return. To more readily apply this yield‐loss rela onship to field scou ng and aphid management, a value in terms of aphids per plant was calculated as the threshold to apply an insec cide to threatening popula ons. That brings us to the economic threshold (ET). This is the key number for management of the pest and is the insect popula on at which management ac on should be applied to prevent a growing popula on from causing economic injury. The ET can also be

In university research across the North Central Region, trea ng below 250 aphids/plant resulted in no observable yield increase, suppor ng the conclusion that very low thresholds or zero tolerance of aphids is not necessary (h ps:// www.ent.iastate.edu/soybeanresearch/content/extension). Again, there are no published, peer‐reviewed data that show that soybean aphid damage is likely below the ET. Therefore, for a posi ve return on investment, treat only the fields that have a reasonable chance of reaching economically damaging levels. Lowering the ET below 250 aphids/plant will not save yield. Instead, it will result in spending money unnecessarily on many more fields that would not have had economic loss from aphid injury. This threshold is conserva ve in that it allows plenty of me for ac on

on the producer’s part before yield loss could begin. This is par cularly true during late soybean growth stages.

COSTS OF TREATING SOYBEAN APHIDS TOO EARLY While some newer insec cides target a narrower range of insects, most insec cide applica ons are not specific. They will kill beneficial insects (lady beetles, parasi c wasps, etc.) as well as pests, later allowing soybean aphid popula ons to rebound in fields without those beneficial insects to slow them down. By using the ET, natural enemies will have a chance to suppress the aphid popula on and possibly prevent it from reaching economically damaging levels. A er applica on, insec cide residues will kill insects for a short me, but insec cide ac vity invariably declines over me (generally, this is considered a good thing). With most insec cides registered for soybean aphid control (such as pyrethroids), soybean foliage emerging a er treatment is not protected. Insec cides that are absorbed and translocated within soybean plants typically move upward only a leaf or two and eventually leave unprotected foliage, especially when applied early in the season. Applying treatments early can result in a false sense of security and a reduced reliance on scou ng. If a re‐infesta on is not detected before reaching the EIL, yield may be reduced. If detected, the cost of addi onal insec cide applica ons are incurred. Early treatment can reduce or eliminate the cost efficiencies of a single, well med threshold‐based treatment. Finally, unnecessary insec cide applica ons do nothing posi ve for a short‐term return on investment. Importantly, long‐term returns can be reduced if insec cide resistance becomes fixed in the soybean aphid popula on. This has happened many, many mes in the history of pest management. We know that managing pes cide resistant pests is seldom "cheap and easy" (for example, consider the problems with herbicide resistant weed control).

HOW DO YOU KNOW IF YOU HAVE A SOYBEAN APHID PROBLEM? All soybean fields are not equally likely to have a soybean aphid problem. Geographic, landscape, biological and agronomic factors all influence soybean aphid popula ons. The research results generated on commercial and University farms across the North Central Region can help iden fy when and where to target early‐ and late‐season aphid scou ng efforts. Early aphid infesta ons are o en found in smaller fields near buckthorn (1) and are o en more abundant near field edges. Soybean aphids prefer moderately dry soil moisture condi ons (20). Soybeans grown in soils tes ng low in potassium contain higher levels of amino acids favorable for soybean aphid development (25) and aphid feeding can intensify potassium deficiency symptoms on these soils. Aphids are o en most abundant in late maturing fields. During vegeta ve growth stages, soybean aphids are o en on the upper, newly expanding leaves. During reproduc ve growth stages, soybean aphids tend to move to leaves, stems and pods lower in the canopy (15). Soybean aphids should be scouted by examining individual plants throughout the field (7). Because soybean aphids remain a ached to the plant while feeding and can occur throughout the canopy, use of a sweep net is not recommended for assessing popula ons of this pest.

It takes me for aphid popula ons to grow. It's important to note that some mes soybean aphid popula ons never grow at all ‐ a single aphid does not invariably lead to hundreds! Soybean aphids can ini ally colonize a field and be rapidly wiped out by a combina on of inhospitable environmental condi ons and predatory insects. Once established, popula ons can grow at a rate where numbers double every 1 ½ days to as many as 6 days depending on environment and natural controls (14, 23). Most o en, research documented that in‐field popula ons doubled every 3 days (23). Soybean fields should be scouted on a regular basis. Soybean aphid popula ons can increase rapidly, par cularly with winged aphids migra ng into fields. Early‐season scou ng can focus on fields with high risk for coloniza on or a history of early coloniza on by aphids. As aphid popula ons develop, more fields should be scouted. There may not be a need to visit every field every week, but fields with a history of high popula ons may need to be scouted weekly or more. The following resources may help to develop an efficient scou ng strategy (Scou ng guide for North Central Region ‐ h ps://www.ent.iastate.edu/soybeanresearch/ files/page/files/SBAFieldGuide%20final.pdf)

BIOLOGY HELPS DETERMINE THE PROFITABILITY OF CROP PRODUCTION ON YOUR FARM: IGNORING BIOLOGY IS EXPENSIVE None of what we have presented here is new, or groundbreaking informa on. However, all of what we have presented here is based on science that has been ve ed and implemented over thousands of acres for more than a decade. Economic injury levels take commodity prices, labor and control costs into account. Fortunately, the biological components of an EIL are not sensi ve to commodity or input prices. The insects on your farm do not eat faster or more when crop prices are high or insec cide costs are low; nor is your crop more sensi ve to insect damage (remember the damage boundary). Yield loss occurs at the same level of pest popula on, regardless of market prices of commodi es. It makes no sense to treat if there is no reasonable likelihood of damage. Science is best when it does not sit s ll. New research on pest and crop biology and on new management tools may change EIL’s and associated ET’s over me. However, since the adop on of the 250 aphid/plant economic threshold, addi onal research has only confirmed the results of the original mul ‐state biological and economic research. While some may view an insec cide cos ng "only a couple of dollars" as inexpensive when compared to other produc on inputs, it is s ll an added cost for no added benefit. These inputs add up with each acre applied. Farmers o en find the "free" applica on costs when insec cides are tank‐mixed with herbicides or other pes cides have unintended nega ve consequences ‐ poor control from poor ming or applica on techniques of one or more products. Using an ET, based on sound, peer‐reviewed research will help you apply your crop input dollars where they are most likely to produce a posi ve return on your investment and minimize the chances of crea ng other problems for yourself. Using fear or faulty economic logic is tried and true as a very effec ve sales tool. It’s always prudent to be a skep cal consumer and consider the messenger when you evaluate informa on ‐ a

conflict of interest can arise if a profit mo ve underpins recommenda ons made without facts behind them. Be very wary of ETs that are based on "feel", eyewitness accounts, or other anecdotes that are not supported by hard scien fic data. ETs that are radically different from those recommended by agricultural research universi es are another red flag. Hopefully, this ar cle has provided you with informa on that will help you sort through the informa on clu er on TV, radio, print media and especially the internet. A list of research references is included for those who would like to read and learn of some of the research suppor ng our soybean aphid management guidelines and economic threshold recommenda ons. Contact Extension for the most up‐to‐date and state‐specific recommenda ons.

Selected references 1) Bahlai, C. A., S. Sikkema, R. H. Halle , J. Newman, and A. W. Schaafsma. 2010. Modeling distribu on and abundance of soybean aphid in soybean fields using measurements from the surrounding landscape. Environmental Entomology 39: 50‐56. 2) Beckendorf, E. A., M. A. Catangui, and W. E. Riedell. 2008. Soybean aphid feeding injury and soybean yield, yield components, and seed composi on. Agronomy Journal 100: 237–246. 3) Davis, J. A., E. B. Radcliffe, and D. W. Ragsdale. 2005. Soybean aphid, Aphis glycines Matsumura, a new vector of Potato virus Y in potato. American Journal of Potato Research 82: 197‐201. 4) Davis, J. A., and E. B. Radcliffe. 2008. The importance of an invasive aphid species in vectoring a persistently transmi ed potato virus: Aphis glycines is a vector of Potato leafroll virus. Plant Disease 92: 1515‐1523.

11) Macedo, T. B., C. S. Bastos, L. G. Higley, K. R. Ostlie, and S. Madhavan. 2003. Photosynthe c responses of soybean to soybean aphid (Homoptera: Aphididae) injury. 2003. J. Econ. Entomology 96: 188‐193. 12) Malumphy, C. P. 1997. Morphology and anatomy of honeydew elimina ng organs, pp. 269–274. In Y. Ben‐Dov and C. J. Hodgson (eds.), So scale insects: their biology, natural enemies and control, vol. 7A. Elsevier Science B.V., Amsterdam, The Netherlands. 13) McCarville, M. T., D. H. Soh, G. L. Tylka, and M. E. O’Neal. 2013. Aboveground feeding by soybean aphid affects soybean cyst nematode reproduc on belowground. PLoS ONE 9: e86415. 14) McCornack, B. P., D. W. Ragsdale, and R. C. Vene e. 2004. Demography of soybean aphid at summer temperatures. Journal of Economic Entomology 97: 854‐861. 15) McCornack, B. P., A. C. Costamagna, and D. W. Ragsdale. 2008. Within‐ plant distribu on of soybean aphid (Hemiptera: Aphididae) and development of node‐based sample units for es ma ng whole‐plant densi es in soybean. Journal of Economic Entomology 101: 1488‐1500. 16) Mi ler, T. E., and A. E. Douglas. 2003. Honeydew. In V. H. Resh and R. T. Carde (eds.), Encyclopedia of Insects. Academic Press, San Diego, CA. 17) Mueller, E. E., and C. R. Grau. 2007. Seasonal progression, symptom development, and yield effects of Alfalfa mosaic virus epidemics on soybean in Wisconsin. Plant Disease 91: 266‐272. 18) Mueller, E. E., K. E. Frost, P. D. Esker, and C. Gra on. 2010. Seasonal phenology of Aphis glycines (Hemiptera: Aphididae) and other aphid species in cul vated bean and noncrop habitats in Wisconsin. Journal of Economic Entomology 103: 1670‐1681. 19) Myers, S. W., and C. Gra on. 2006. Influence of potassium fer lity on soybean aphid popula on dynamics at a field and regional scale. Environmental Entomology 35: 219‐227.

5) Douglas, A. E., and H. F. van Emden. 2007. Nutri on and symbiosis. In H. van Emden and R. Harrington (eds), Aphids as Crop Pests, CAB Interna onal, Oxfordshire, UK.

20) Nachappa P., C. T. Culkin, P. M. Saya II, J. Han, and V. J. Nalam. 2016. Water stress modulates soybean aphid performance, feeding behavior, and virus transmission in soybean. Fron ers in Plant Science 7: 552. DOI: 10.3389/fpls.2016.00552.

6) Hill, J. H., R. Alleman, D. B. Hogg, and C. R. Grau. 2001. First report of transmission of Soybean mosaic virus and Alfalfa mosaic virus by Aphis glycines in the New World. Plant Disease 85: 561. DOI: 10.1094/ PDIS.2001.85.5.561C.

21) Pe ersson, J., W. F. Tjallingii, and J. Hardie. 2007. Host‐plant selec on and feeding. In H. van Emden and R. Harrington (eds), Aphids as Crop Pests, CAB Interna onal, Oxfordshire, UK.

7) Hodgson, E. W., B. P. McCornack, K. Tilmon, and J. J. Knodel. 2012. Management recommenda ons for soybean aphid (Hemiptera: Aphididae) in the United States. Journal of Integrated Pest Management DOI: 10.1603/ IPM11019. 8) Insaus , P., E. L. Ploschuk, M. M. Izaguirre, and M. Podworny. 2015. The effect of sunlight intercep on by sooty mold on chlorophyll content and photosynthesis in orange leaves (Citrus sinensis L.). European Journal of Plant Pathology 143: 559‐565. 9) Krupke, C., W. Bailey, C. DiFonzo, E. Hodgson, T. Hunt, K. Jarvi, B. Jensen, J. Knodel, R. Koch, B. McCornack, A. Michel, J. Peterson, B. Po er, A. Szczepaniec, K. Tilmon, J. Tooker, and S. Zukoff. 2015. The effec veness of neonico noid seed treatments in soybean, 8 pp. Purdue University, Publica on E‐268. 10) Lemos Filho, J. P., and E. A. S. Paiva. 2006. The effects of sooty on photosynthesis and mesophyll structure of mahogany (Swietenia macrophylla King., Meliaceae). Bragan a 65: 11‐17.

22) Pedigo, L. P., S. H. Hutchins, and L. G. Higley. 1986. Economic injury levels in theory and prac ce. Annual Review of Entomology 31: 341‐368. 23) Ragsdale, D. W., B. P. McCornack, R. C. Vene e, B. D. Po er, I. V. MacRae, E. W. Hodgson, M. E. O’Neal, K. D. Johnson, R. J. O’Neil, C. D. DiFonzo, T. E. Hunt. P. A. Glogoza, and E. M. Cullen. 2007. Economic threshold for soybean aphid. Journal of Economic Entomology 100: 1258‐ 1267. 24) Ragsdale, D. W., D. A. Landis, J. Brodeur, G. E. Heimpel, and N. Desneux. 2011. Ecology and management of the soybean aphid in North America. Annual Review of Entomology 56: 375‐399. 25) Walter, A. J., and C. D. DiFonzo. 2007. Soil potassium deficiency affects soybean phloem nitrogen and soybean aphid popula ons. Environmental Entomology 36: 26‐33. 26) Wang, R. Y., A. Kritzman, D. E. Hershman, and S. A. Ghabrial. 2006. Aphis glycines as a vector of persistently and nonpersistently transmi ed viruses and poten al risks for soybean and other crops. Plant Disease 90: 920‐926.

for more informaƟon: hƩp://www.extension.umn.edu/agriculture/ © 2017, Regents of the University of Minnesota. University of Minnesota Extension is an equal opportunity educator and employer. In accordance with the Americans with Disabili es Act, this publica on/material is available in alterna ve formats upon request. Direct requests to 612‐624‐0772 or [email protected].

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