Source: PURDUE UNIVERSITY submitted to NRP
NEONICOTINOID SEED TREATMENTS IN BT MAIZE: BALANCING CONTRIBUTIONS TO INSECT RESISTANCE MANAGEMENT WITH IMPACTS ON SOIL HEALTH
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1013715
Grant No.
2017-33522-27103
Cumulative Award Amt.
$500,000.00
Proposal No.
2017-03801
Multistate No.
(N/A)
Project Start Date
Sep 1, 2017
Project End Date
Aug 31, 2022
Grant Year
2017
Program Code
[HX]- Biotechnology Risk Assessment
Recipient Organization
PURDUE UNIVERSITY
(N/A)
WEST LAFAYETTE,IN 47907
Performing Department
Entomology
Non Technical Summary
Proteins from the soil bacterium Bacillus thuringiensis (B.t.) offer high specificity in insect toxicity. Genes that induce crop plants to express these insecticidal proteins have been successfully inserted into corn and cotton. The vast majority of corn (over 80%) planted in the US expresses at least one Bt toxin for insect management. While this approach has largely been successful on a number of fronts, problems with resistance development by target pests are a constant threat, as they are with constant exposure to any pest management approach.Insect resistance management plans have been implemented to delay the onset of resistance targeting the corn rootworm complex. A mandatory refuge that consists of corn plants that do not express the Bt toxin must be part of every Bt corn planting. This ensures that susceptible insects will always be present to mate with any that survive Bt exposure - effectively "diluting" the population of resistant insects. In other words, this approach seeks to have abundant, susceptible, insects from refuge plants without the pest-specific toxin mating with relatively rare, resistant, insects from toxin-producing plants ("Bt" plants). However, prior research from our group on the key pest of corn, the western corn rootworm (WCR), showed that the numbers of insects generated in currently implemented refuges are insufficient to mate with those emerging from Bt corn in the same field. One possible factor limiting adult emergence from refuge plants are the neonicotinoid insecticides applied to seed. Currently, all Bt corn is sold with neonicotinoid seed treatments (NSTs).Despite this widespread use, the contribution of NSTs to corn rootworm control (including resistance management) in Bt corn is completely unknown. For example, the insecticide may be detrimental to resistance management, by causing mortality in the refuge insects that we are trying to preserve. On the other hand, there are other, non-rootworm soil pests that can be effectively managed with NSTs. We will examine the economic need for NSTs to prevent root injury and yield loss from soil insects in two ecologically distinct states where root feeding insect pests routinely occur, Indiana and Virginia.Aside from hybrid differences, most corn in the US is grown using very similar approaches - both expressing Bt toxins and using NSTs. However, the below-ground pest complexes are very different: corn rootworms dictate pest management in Indiana, whereas wireworms, white grubs, and rootworms are concerns in Virginia. While abundant data on environmental impacts exist for Bt products, the costs/benefits of persistent NST residues on soil health have not been measured - Objective 1 of our proposed work will fill this information gap. Using novel methods developed by our group, we will measure rootworm emergence from refuges with and without NSTs, then characterize the value of the control NSTs provide by complementing insect-resistant Bt maize hybrids. During Objective 2, we will collect data on insecticide residues in soil and water in these experiments. We hypothesize that NSTs can be removed from GM corn seeds grown in some regions without increase in pest damage or diminished refuge function (i.e., number of insects produced from refuge plants). Further, we hypothesize that removing NSTs will have the potential for a beneficial effect upon soil and watershed health via reduced residues. The overall goal of this research is to provide information to guide the use of NSTs in a way that does not compromise refuge function, while providing growers protection from root-feeding pests where appropriate. Reductions of levels of pesticide in soil is a stated goal of the 2017 BRAG program as well. The proposed work is directly applicable to the following specified areas from the BRAG 2017 RFA: Environmental impacts of GE relative to non-GE organisms in the context of production systemsc) Comparative assessment of environmental impacts of agricultural production systems using organic and/or conventional methods with those involving plant, animal, or biotechnology.
Animal Health Component
75%
Research Effort Categories
Basic
25%
Applied
75%
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
21115101130100%
Goals / Objectives
Objective 1: Quantify effects NSTs on refuge performance, Years 1-3We will measure the production of refuge insects and mating between refuge and Bt insects in corn fields. This will accomplished by collecting data on emergence and mating rates of refuge/Bt insects in 5% seed blends. We will determine if removing NSTs 1) disproportionally affects the respective population sizes of Bt/refuge insects; and 2) affects how often insects from different hosts mate.Objective 2: Quantify the relative benefit of NSTs in combination with Bt toxins for management of WCR and other soil pests, Years 1-3In this objective we will determine the contribution of each approach (Bt vs. NSTs vs. both) to pest management in the field in both VA and IN. This will allow us to test different pest complexes in different regions and growing conditions and document whether effects of both approaches are additive, synergistic or neutral.Objective 3: Quantify the levels of insecticide residues found in soil and water collected from fields planted with and without NSTs, Years 2-3.Using the same fields as experiments outlined above, we will determine whether insecticide residues change significantly as a function of pest management approach. Because we will already have data on pest management efficacy from Objective 1 and 2, this work will allow us to include a previously uninvestigated parameter of NST use, namely the accumulation (or lack thereof) of insecticide residues in soil and water in and near production fields).
Project Methods
Objective 1: Quantify effects NSTs on refuge performance Years 1-3All experiments will be conducted in corn fields in both VA and IN (four locations/state). Treatments include: 1) untreated seed, 5% refuge; 2) NST 1.25 mg/kernel clothianidin, 5% refuge. The manufacturer premixes seeds for seed blend refuges. In order to create pure stands of Bt plants, only seeds containing rootworm-specific Bt traits will be initially planted. Seeds will be separated visually by color; seeds that contain the rootworm-specific Bt trait are a different color (typically green) than refuge seeds (typically purple). Immediately following planting, 345 randomly chosen seeds (representing 5% of the 6,900 seeds used per plot, based on planting rate of 27,700 seeds per acre) will be removed and replaced with two refuge seeds. Refuge plants will be labeled with 15N, as follows: an aqueous solution of ammonium nitrate 15N (~98% 15N) (Cambridge Isotope Laboratories, Inc. Andover, MA) and distilled water will be applied as a soil drench to a 1 cm deep hole at the base of refuge plants in the V2 stage using a CO2-pressurized backpack sprayer. A rate of 0.6125 g of ammonium nitrate (~98% 15N; Cambridge Isotopes) per liter of dH20 will used; 10 mL of solution will added to each refuge plant.We will sample eight rows per plot three times per week beginning at appearance of the first adult rootworm beetle in each location. Plots and rows will be sampled in random order. Beetles will be collected into plastic bags and labeled with the date and location; mating pairs will be stored together until processing. Samples will be stored at -20°C.Stable isotope testingWe will use only elytra and head capsules from beetles for isotope analysis to avoid nitrogen from plant matter in the digestive tract and, in females, nitrogen received from male spermatophores during mating (Murphy and Krupke, 2011). Dried elytra and head capsules will be crushed between layers of wax paper, weighed to the nearest 0.001 g and placed into 4 x 6 mm mass spectrometry tin capsules (Costech Analytical Technologies, Inc., Valencia, CA). We will use fresh wax paper for each sample and clean all instruments and workspace with >70% ethanol between samples. The Purdue Stable Isotope Laboratory (Isotope Ratio Mass Spectrometer-IRMS) will perform mass spectrometry testing.Objective 2: Quantify the relative benefit of NSTs in combination with Bt toxins for management of WCR and other soil pests, Years 1-3Treatments include: 1) untreated, Bt seed; 2) NST, Bt seed; 3) untreated, non-Bt seed; 4) NST, non-Bt seed. We will measure root damage in each plot twice, ca. July 20 and Aug 1. At each interval, four consecutive plants/row (two Bt and two refuge) will be removed from 10 rows and root injury assessed following the 0-3 node injury scale, the standard approach for measuring insect feeding. Plants will be harvested, and yield and grain moisture measured, between mid and late September. Secondary soil pests (wireworms, white grubs) and their damage will be assessed by counting the number of plants in 12.2 m of row from one of the center two rows in each plot and converting this value to plants per hectare.At the same time, we will assess the presence and abundance of non-WCR soil pests, by taking soil samples from four locations in each plot prior to planting. We will sample for soil insects by excavating a 20 cm by 15 cm deep volume of soil and sifting it for insect larvae. We will identify insect larvae to species. Grain moisture and yield estimates will be obtained from the two center rows using a Kincaid® 8-XP plot combine.Objective 3: Quantify the levels of insecticide residues found in soil and water collected from fields planted with and without NSTs, Years 2-3.We will conduct these experiments in plots described above. A "reference site," as a negative control, will be located at a forested area near (<10 kilometers) field plots. Plots will be assessed for residues of clothianidin, the NST used in our field plots and the most commonly NST used on corn. ZIn addition, we will measure residue levels in soils and surface water from a wide range of sites (wetlands, streams, ditches) within Indiana and Virginia that are located near corn, soybean and/or fresh market crops to capture a range of potential neonicotinoid residue levels. A critical question regarding neonicotinoid residues is whether residues in agricultural ditches increase or decrease during storm events and how those levels ebb and flow throughout the growing season. Soil samples will be collected from 4 cm below the soil surface to avoid sampling topsoil. Using 10 cm diameter x 15 cm soil cores, we will collect samples at five random locations in the field. These samples will be combined in a 3.78 liter bucket, mixed, and a subsample of the pooled soil transported to the lab in paper bags stored in coolers to minimize the possibility of photolysis. Samples will be stored at -20°C until analysis. Water samples will be collected from ditches and waterways adjacent to fields, using 1-L amber glass bottles and transported to the laboratory on ice. Water samples will be processed within 96 h after collection. Where necessary, the pesticides will be extracted from the matrix (i.e., soil) by agitation with water, acetonitrile and the salts magnesium sulfate and sodium acetate. After centrifuging, a portion of the supernatant acetonitrile layer containing the pesticides can be further cleaned by the addition of solid phase dispersants (primary secondary amine, magnesium sulfate, C-18 silica).

Progress 09/01/17 to 08/31/22

Outputs
Target Audience:Target audiences include a range of professionals affiliated with insect pest management in corn production, including seed dealers, ag-chem dealers and independent consultants. Additional audiences include fellow research and extension scientists working in Bt corn systems. Changes/Problems:The pandemic presented challenges and effectively added a full calendar year onto the project, but in the end we were able to achieve the goals and add to our understanding of Bt corn/refuge management and the effects of NSTs upon this system. What opportunities for training and professional development has the project provided?Kyle Bekelja (PhD, 2021) and Kathleen Miller (MS, 2021) both worked on this project and were largely supported by this grant award. How have the results been disseminated to communities of interest?Throughout the project (with the notable exception of the COVID years), these data were shared by four individuals working on the project at a wide range of research and extension venues, many are summarized in previous reports. Dr. Krupke and Dr. Taylor both lead applied research programs in IN and VA, respectively, and this project was a focal point of in-person and remote extension presentations. Kyle Bekelja and Kathleen Miller both presented these data at professional meetings, most recently the joint meeting of the Entomological Society of America and Canada in Vancouver, British Columbia in November of 2022. Miller, K. and C. Krupke. 2022. Assessment of the influences of neonicotinoid seed treatments of Bt maize upon resistance management. Symposium oral presentation. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? The project delivered on all three research objectives, as follows: Objective 1: Quantify effects NSTs on refuge performance. Our work was the first to separate the contributions of NSTs routinely applied to corn seeds from the Bt toxin, in order to determine if the refuge seeds actually would benefit from not having the NST component. What we found is that the NSTs do not result in any significant increase in refuge beetle populations, nor do they result in significant plant protection from RW feeding. This raises questions about whether NSTs are needed or helpful at all from a pest management/crop protection standpoint. Objective 2: Quantify the relative benefit of NSTs in combination with Bt toxins for management of WCR and other soil pests In both VA and IN, we found that secondary pest numbers were routinely too low to challenge corn plant growth and development. However, where we had some secondary pest infestations we also did not detect any signficant benefits of NSTs on corn seeds. This may be largely due to a lack of pest pressure, resulting in no statistical power to detect differences (i.e. too many zeroes). This does raise questions about the function of NSTs in crop protection from non-rootworm pests in our study areas Objective 3: Quantify the levels of insecticide residues found in soil and water collected from fields planted with and without NSTs Insecticide residue levels were highest in water and soils in/near plots that included NST-treated corn seeds. This is not surprising and has been documented by other published studies. However, it is a useful data point in the discussion of the costs vs. benefits of NST use in Bt corn hybrids. In our study, we were not able to reliably or consistently find benefits in terms of either crop protection or refuge function. The finding that NSTs move offsite and into tile-drained water sources is an important drawback of this approach to deploying insecticides.

Publications

  • Type: Journal Articles Status: Awaiting Publication Year Published: 2023 Citation: Bekelja, K., Miller, K., Taylor, S.V., Kuhar, T., and C. Krupke. 2023. "Removing Neonicotinoid Seed Treatments Has Negligible Effects on Refuge Function and Crop Protection in Transgenic Maize Targeting Western Corn Rootworm (Coleoptera: Chrysomelidae)" Journal of Economic Entomology.
  • Type: Journal Articles Status: Other Year Published: 2023 Citation: Miller, K., Bekelja, K., Taylor, S.V. and C. Krupke. 2023. "Efficacy and non-target effects of neonicotinoid seed treatments in Bt corn/refuge plantings" In prep., journal TBD


Progress 09/01/20 to 08/31/21

Outputs
Target Audience: Nothing Reported Changes/Problems:The major change, and reason for the NCE request, is the delay in availability of the core facility that processes our water and soil samples. This is beyond our control, and many researchers use this facility and are delayed as a result of the mandatory pandemic closures for most of the last 18 months or so. What opportunities for training and professional development has the project provided?One graduate student in Indiana (Kathleen Miller) and one graduate student in Virginia (Kyle Bekelja) were funded under this grant. Both are expected to defend and graduate in late 2021 (Miller) or early 2022 (Bekelja). How have the results been disseminated to communities of interest?Nothing to report for this period, please see previous reports for oral and poster presentations during the life of the project. What do you plan to do during the next reporting period to accomplish the goals?We are currently on track to complete analysis of soil and water samples for Virginia at the Purdue core facility by end of 2021, which has been mostly closed or restricted access for the last 18 months. This delay is the reason for the no-cost extension request. Once the data are in our hands, statistical analysis and write-up can proceed and the Virginia student (Bekelja) can defend and graduate in early 2022.

Impacts
What was accomplished under these goals? All fieldwork and sample collections are complete. The current status of the work is waiting to complete analyses at a core facility for Objective 3, this is the reason for the no-cost extension request.

Publications


    Progress 09/01/19 to 08/31/20

    Outputs
    Target Audience:The target audiences are agricultural professionals, fellow researchers and extension staff. Changes/Problems:As with virtually all researchers worldwide, the pandemic affected our ability to complete most tasks. This was particularly evident in lab residue analyses, where our principal facility was shut down for several months. However, we were able to modify activities and salvage a final field season in Indiana, and at this writing (December 2020) are completing our lab analyses. What opportunities for training and professional development has the project provided?Two graduate students (Kyle Bekelja in VA, Kathleen Miller in IN) were supported as part of this grant and worked on all three objectives in their respective states. Both are expected to defend their theses in 2021 and publish the work that formed the core of this proposal. How have the results been disseminated to communities of interest?Please see "products" section for a sampling of talks given by graduate student Bekelja and co-PI Taylor. What do you plan to do during the next reporting period to accomplish the goals?Complete all analyses in lab and write-up of final results. We anticipate completing all project work in early 2021.

    Impacts
    What was accomplished under these goals? We completed the field work for the final year of each objective in both IN and VA. We are currently completing analysis of IN beetle collections (N15 head capsule analysis) and soil and water samples (Obj 1 and 3, respectively). We are completing analysis of water samples for VA in Objective 3. We anticipate all analyses will be completed during the first half of 2021, barring any pandemic-related facility shutdowns.

    Publications


      Progress 09/01/18 to 08/31/19

      Outputs
      Target Audience:The target audiences are agricultural professionals, fellow researchers and extension staff. Changes/Problems:Virginia: Similar to weather conditions in 2018, we experienced heavy rainfall and flooding in Blacksburg during May and June 2018. One plot of neonicotinoid treated seed was extensively damaged and no beetles emerged from this field. Indiana: One of the wettest springs in 30 years resulted in very late planting. However, rootworm beetle numbers were still surprisingly robust. However, this might have affected secondary pest timing (Obj. 2). What opportunities for training and professional development has the project provided?A graduate student, Kyle Bekelja, is leading this work at the Virginia site and was involved in all field sampling reported here. He has transitioned to the PhD program and will continue to work on this project in 2020. He presented his research at the 2018 Entomological Society of America meeting and was awarded first place in the MS Oral Presentation Student Competition. He currently supervises two undergraduate researchers. Kathleen Miller is a graduate student leading the work in Indiana. She will continue this work in 2020-21. She also supervised two undergraduate technical assistants on the project. How have the results been disseminated to communities of interest?Virginia: Results were presented in producer meetings in Dec - Feb 2019. Personal phone calls have been made to affected producers, Cooperative Extension Agents, and seed/insecticide distributors to discuss seed and insecticide purchasing for next season. What do you plan to do during the next reporting period to accomplish the goals?Virginia: Water samples for 2019 and soil samples from 2018 and 2019 will be processed and analyzed. Indiana: complete Obj. 1 and Obj. 3 analyses for 2019 data.

      Impacts
      What was accomplished under these goals? Objective 1: Quantify effects NSTs on refuge performance, Years 1-3 Virginia: Research experiments were planted at the Kentland Research Farm in Blacksburg, Virginia. Plots were planted in late May due to excessive rainfall. Adult western corn rootworm individuals and mating pairs were collected from these plots between July and August 2019. Beetles were returned to the laboratory, measured to assess relative fitness (e.g., head capsule size, dry weight), and prepared for isotope analysis. One hundred thirty-five beetles were analyzed from 2018 and 104 beetles were analyzed from 2019. In 2018, refuge insects represented 28% of the population in untreated plots and 38.5% of the population in treated plots. In 2019, refuge insects represented 17% of the population in untreated plots and 2% of the population in the treated plots. In late-July, roots from corn plants in all research plots were rated for rootworm injury. On average, injury did not exceed economic threshold. Injury in Bt corn treated with neonicotinoids, Bt corn without neonicotinoids and refuge corn treated with neonicotinoids was not different. Injury in untreated refuge corn were different from Bt corn with and without neonicotinoids and refuge corn with neonicotinoids (p<0.05). Indiana: Research experiments were planted at two locations in Indiana, and plots were planted in early June due to excessive rainfall. Adult western corn rootworm individuals and mating pairs were collected from plots between July and September 2019. Beetles were returned to the laboratory, measured to assess relative fitness (e.g., head capsule size, dry weight), and prepared for isotope analysis.1029beetles collected,27mating pairs etc. In August(8/12, 8/13, 8/20), roots from corn plants in all research plots were rated for rootworm injury.On average, injury did not exceed economic threshold. Objective 2: Quantify the relative benefit of NSTs in combination with Bt toxins for management of WCR and other soil pests, Years 1-3 Virginia: Soil samples were taken to determine insect pest presence at planting. Wireworm and white grub species were collected and identified. Plots averaged 0.71 wireworms per sample and 0.37 white grubs. Indiana: Soil samples were taken to determine insect pest presence at planting. Wireworm and white grub species were collected and identified. Plots averaged 0.003 wireworms per sample and 0.11 white grubs. Objective 3: Quantify the levels of insecticide residues found in soil and water collected from fields planted with and without NSTs, Years 2-3. Virginia: Water samples from upstream and downstream of the research farm at the closest running water source were taken. Samples were also taken of surface water in fields following rainfall events. These samples are currently being processed for insecticide residue analysis. Samples were analyzed from 2018. Low levels of residues (<0.01 ng/ml) were detected in stream water upstream and downstream of the research station. Downstream concentrations were higher following planting. Clothianidin residues in surface water from the untreated plot (0.1533 ng/mL) were lower than the treated plot (0.3409 ng/mL). Indiana: Water samples from upstream and downstream of the research farm at the closest running water source were taken. These samples are currently being processed for insecticide residue analysis.

      Publications


        Progress 09/01/17 to 08/31/18

        Outputs
        Target Audience:Target audience includes field crop producers, consultants, ag-chem industry personnel, extension educators and other researchers. Changes/Problems:Virginia: We experienced heavy rainfall and flooding in Blacksburg during May and June 2018. One plot of neonicotinoid untreated seed was extensively damaged and no beetles emerged from this field. Because of the inability of equipment to enter the field, no supplemental nitrogen was applied and yield measurements were not taken. Indiana: As in previous years, rootworm numbers were very low statewide. We took steps to remedy this by planting highly attractive pollen sources (pumpkins) in plots in 2018 to attract females to lay eggs to heighten 2019 populations. What opportunities for training and professional development has the project provided?A graduate student, Kyle Bekelja, is leading this work at the Virginia site and was involved in all field sampling reported here. He is expected to continue with this in 2019 and ultimately this work will form the basis of his Masters thesis. How have the results been disseminated to communities of interest?Virginia: Mounting reports of rootworm feeding upon Bt hybrids have made this project especially timely in the region. Producer meetings to discuss mitigation strategies for current resistance issues have been scheduled for Jan - Feb 2019. Personal phone calls have been made to affected producers, Cooperative Extension Agents, and seed/insecticide distributors to discuss seed and insecticide purchasing for next season. We will finish isotope and residue analysis of existing soil/water/insect samples in fall 2018/spring 2019. Field experiments will be replicated in Virginia in 2019. Information will continue to be made available in a timely manner through updates, management recommendations, and educational programs for the target audiences. Indiana: The rootworm objectives (1 and 2) were not conducted in 2018. No reports of rootworm feeding upon Bt corn hybrids have been documented in the state. What do you plan to do during the next reporting period to accomplish the goals?Virginia and Indiana: replicate Objectives 1-3 in 2019.

        Impacts
        What was accomplished under these goals? Objective 1: Quantify effects NSTs on refuge performance, Years 1-3 Indiana: Fields were selected and planted to corn for 2019 planting of this objective at both TPAC and PPAC research farms. Field logistics made it necessary for Indiana to conduct this objective in Years 2 and 3 to maximize probability of rootworm infestation and usable data. Virginia: Research experiments were planted at the Kentland Research Farm in Blacksburg, Virginia. Adult western corn rootworm individuals and mating pairs were collected from these plots between July and August 2018. Beetles were returned to the laboratory, measured to assess relative fitness (e.g., head capsule size, dry weight), and are currently being prepared for isotope analysis. In late-July, roots from corn plants in all research plots were rated for rootworm injury. On average, injury did not exceed economic threshold. Injury in Bt corn treated with neonicotinoids and refuge corn treated with neonicotinoids was not different. Injury in Bt and refuge corn treated with neonicotinoids and untreated Bt corn were different from untreated refuge corn (p<0.05). In July and August 2018, corn plant lodging in association with high numbers of western corn rootworm adults was reported by growers and Cooperative Extension agents in western VA and NC. Root ratings were taken from these fields. In the five fields visited, root injury averaged between 1-2 nodes injury. Fields were planted to either Agrisure (mCry3A) or Yieldgard (Cry3Bb1) varieties. Objective 2: Quantify the relative benefit of NSTs in combination with Bt toxins for management of WCR and other soil pests, Years 1-3 Indiana: Two sites were planted and monitored throughout the season, PPAC and TPAC research farm. Low levels of damage and pest infestations throughout the season, although wireworms and white grubs were found consistently (several species of both) they were not found to be feeding on plants and were typically far from the root masses when found. Virginia: Soil samples were taken to determine insect pest presence at planting. Wireworm species were collected and identified. Objective 3: Quantify the levels of insecticide residues found in soil and water collected from fields planted with and without NSTs, Years 2-3. Indiana and Virgina: This objective was conducted as planned at all locations in 2018. Water and soil samples were collected from the experiment field and water samples from upstream and downstream of the research farm at the closest running water source. These samples are currently being processed for insecticide residue analysis.

        Publications