Progress 02/01/24 to 01/31/25
Outputs
Target Audience:The target audience for this proposal includes extension educators and scientists from academia, industry, and the government. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?This project has provided training opportunities for one postdoctoral research scientist (Dr. Margaret Lewis), who assumed primary responsibility for all aspects of the project management starting in August 2023. Four undergraduate students (Dylan Murray, Tori Elek, Jordan Lehman, and Cy Marchese) also assisted with various aspects of data collection for this project. In addition to developing their laboratory research skills, the students also have participated in various professional development opportunities. For example, Lehman and Marchese attended an extension meeting in 2023 that focused on how climate and extreme weather events might impact agriculture. Lehman has also developed a plan for an independent undergraduate research study based off Objective 2 of this project, and she successfully applied for and received a competitive undergraduate research fellowship through OSU. This fellowship provided summer salary support for Lehman in Summer 2024. Lehman and Murray have also contributed to manuscript preparation for the parasitoid experimental work (Objective Two), building their skills in data analysis and scientific writing. They will eventually be included as co-authors on the resulting publication. Three graduate students (Aniket Banerjee, Urvashi Verma, Kanishka Goyal) also led efforts to develop mathematical models. They have met with Dr. Margaret Lewis on a bi-weekly basis, so as to understand the ecological and entomological features of the various objectives, to model them accurately, in mathematical models. This has greatly benefitted their interdisciplinary training. They met regularly with Dr. Rana Parshad, to fine tune the modeling nuances, as part of their PhD training. How have the results been disseminated to communities of interest?Research results have been broadly disseminated to academic communities at regional, national, and international scientific conferences, including: Midwest mathematical Biology Conference (4 talks, May 2024, La Crosse, WI) Society of Industrial and Applied Mathematics national meeting (2 talks, June 2024, Portland, OR) 9th Annual meeting of SIAM Central States Section, (2 talks, October 2024, University of Missouri, Kansas City) 2024 Climate and Soybean Pests Webinar (hosted by Ohio State University Extension) What do you plan to do during the next reporting period to accomplish the goals? Identify a molecular marker for differentiating between soybean aphid biotypes using RadSeq. Use marker to finish processing mixed soybean aphid mesocosm samples (Objective 3). Perform biochemical analyses to quantify how flooding stress impacts on aphids as a host for parasitoids. Analyze composition and quantity of amino acids and secondary metabolites in aphid samples (collected during Year 2 of this project). Finish writing and submit manuscripts related to Objective 1 (Aphid Life Tables), Objective 2 (water stress and aphid-parasitoid interactions) and Objective 4 (soybean aphid biocontrol models). Develop models to quantify how water stress impacts soybean aphid biological control, building upon the models that were developed during Year 2 of this project. Continue to work further with non-autonomous (that is time dependent) models, as well as models with time delay, as well as models with structure. A pivotal goal for the next year is to prove the existence of oscillations seen in the models developed, as well as to quantify their appearance and timing - so as to devise better tactics and strategies via these models foe pest management.
Impacts
What was accomplished under these goals?
Mesocosm assays were conductedusing two soybean varieties, an aphid-susceptible soybean variety and a near isoline soybean variety that was bred to express Rag1+2 aphid resistance genes. Flooding decreased avirulent aphid population densities by 28% and 44% on susceptible and Rag1+2 soybean varieties respectively, but it had not impact on virulent aphid populations. These results are consistent with our hypothesis that flooding stress in soybeans only has a negative impact on avirulent soybean aphid populations. This phenotypic data was incorporated into a manuscript that examines flooding impacts on the soybean aphid transcriptome and was accepted for publication in Scientific Reports (Lewis et al. 2025). This data has also been used to guide the development of mathematical models that quantify flooding impacts on aphid population dynamics (Banerjee et al. 2025). Life table experiments were conducted using only the aphid-susceptible soybean variety. In previous mesocosm assays, we had observed similar responses to flooding regardless of soybean variety, and using only one soybean variety reduced the number of treatment combinations, allowing for more robust replication (20 - 25 replicates per treatment combination). No changes in development time or longevity were noted for either virulent or avirulent aphid biotypes. In contrast, total aphid fecundity in avirulent aphids decreased from 39.26 ± 3.24 (mean ± standard error) nymphs per adult to 32.11 ± 2.97 nymphs per adult under flooding conditions. No drop in fecundity was noted for the virulent aphid biotype. This data will be included as part of a manuscript that is currently in preparation for the journal Environmental Entomology (target submission date Summer 2025). Laboratory assays were quantified to evaluate how flooding stress alters interactions between soybean aphids and parasitoids (Aphidius colemani), including no-choice assays to quantify parasitoid fitness and behavioral assays to determine if flooding alters parasitoid host acceptance (Objective 2). We conducted no-choice laboratory assays to examine how host plant flooding stress impacts parasitoid fitness, Experiments were conducted using both virulent (Biotype 4) and avirulent (biotype 4) soybean aphid nymphs. To understand the mechanism underlying potential differences between water-stressed and non-water stressed aphids as hosts for parasitoid wasps, we also performed laboratory assays to quantify aphid host quality. Briefly, aphid nymphs were reared on flooded or optimally watered soybean plants for seven days. Behavioral observations were also performed to determine if host plant water stress influenced parasitoid preference for aphids. We monitored interactions between a mated, female parasitoid wasp and a soybean aphid that had been reared on either a water-stressed soybean plant or an optimally watered plant (control). In each experimental unit (i.e. one aphid - parasitoid pair), behavior was recorded for five minutes or until a successful parasitoid attack occurred. Results: Overall, our data to date suggests that flooding stress benefits the aphid parasitoid. We found no differences in the size of aphid hosts as a result of flooding, suggesting that reduced parasitoid emergence rates are not a result of resource limitation (i.e. smaller hosts). Instead, it is possible that changes to the aphid metabolomic profile and/or suppressed aphid immunological responses are driving these phenotypic changes. Future work will be necessary to confirm this hypothesis. Data collection for the no-choice parasitoid assays is complete. Co-PI M. Lewis is currently supervising two undergraduate students (Jordan Lehman and Dylan Murray) in manuscript preparation. We are targeting a Fall 2025 submission date. We began collecting samples for laboratory mesocosm assays with mixed virulent and avirulent aphid populations (Objective 3); Aphid samples are currently being stored in a -20C freezer; we are currently working to develop a molecular marker that will allow us to distinguish between biotypes using a PCR or restriction enzyme digest based assay. Once those markers are developed, we will be able to process our freezer aphid samples, allowing us to determine the proportion of virulent and avirulent aphids present in a population. Mathematical models (Objective 4) were developed to predict water stress impacts on virulent and avirulent soybean aphid population dynamics. The classical boom-bust models (with one peak) that are commonly used to replicate/predict aphid population dynamics may not reflect dynamic field conditions, because abiotic factors such as extreme weather events could lead to more than one population peak in a growing season. We therefore investigated models that have multiple peaks, including a basic one species model that uses a variable, time-dependent carrying capacity to replicate flooding stress impacts on aphid population dynamics. Refined models were published in the journal Mathematic Biosciences and Engineering (Banerjee et al. 2025). We are currently working to develop models that quantify interactions between soybean aphids and their natural enemies. These models broadly aim to compare the efficacy of two different types of biological control agents: a parasitoid wasp (Aphidius colemani) and a generalist predator (green lacewing larvae). Specific scenarios include models with a single natural enemy (soybean aphid + parasitoid wasp or soybean aphid + generalist predator) as well as a model with two natural enemies present (soybean aphid + parasitoid wasp + generalist predator) to quantify impacts due to intraguild predation. The models developed are age structured models that break up the aphid and enemy populations into appropriate ages, such as juveniles (in several instar stages) and adults, to more accurately model the biology. For example our laboratory experiments show parasitoids prefer aphids in the third and fourth instar - this preference has been modeled into our current model systems. We have also modeled the use of insecticides such as neonicotinoids on aphid control. These are modeled as non-autonomous or time dependent systems, depending on the frequency of the application. A key finding from the long term simulation of our models, is that top down predator control, as well as insecticide use can lead to chaos or transient chaos, that causes aperiodic dynamics in the populations - however, when a combined predator-parasitoid model is used, the dynamics can be stabilized. These findings via modeling are matched to actual field data on aphids and their enemies in the 2000-2015 period, and match the field data accurately. Laboratory assays have also been conducted to guide model development and to validate model results. For example, we evaluated how aphid development stage impacts parasitoid attack rate and conducted functional response assays to measure lacewing larvae consumption of soybean aphids. A manuscript detailing these model results is currently in preparation, with anticipated submission in spring 2025 (target journal is the Journal of Economic Entomology). These models will provide a foundation for future modeling efforts that quantify how water stress might alter aphid - natural enemy interactions.
Publications
- Type:
Peer Reviewed Journal Articles
Status:
Published
Year Published:
2025
Citation:
Lewis, M.T., Poelstra, J.W., and A.P. Michel. 2025. Host plant flooding stress in soybeans differentially impacts avirulent and virulent soybean aphid (Aphis glycines) biotypes. Scientific Reports. 15: 4897. https://doi.org/10.1038/s41598-025-87561-z
- Type:
Peer Reviewed Journal Articles
Status:
Published
Year Published:
2025
Citation:
Banerjee, A., Verma, U., Lewis, M.T., and R. Parshad. 2025. Two species competition with a non-smooth Allee mechanism: applications to soybean aphid population dynamics under climate change. Modern Trends in Mathematical Ecology. 22: 604-651.
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Progress 02/01/23 to 01/31/24
Outputs
Target Audience:The target audience for this proposal includes extension educators and scientists from academia, industry, and the government. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?This project has provided training opportunities for one postdoctoral research scientist (Dr. Margaret Lewis), who assumed primary responsibility for all aspects of the project management starting in August 2023. Four undergraduate students (Dylan Murray, Tori Elek, Jordan Lehman, and Cy Marchese) also assisted with various aspects of data collection for this project. In addition to developing their laboratory research skills, the students also have participated in various professional development opportunities. For example, Lehman and Marchese attended an extension meeting in 2023 that focused on climate change impacts on agriculture. Lehman has also developed a plan for an independent undergraduate research study based off Objective 2 of this project, and she successfully applied for and received a competitive undergraduate research fellowship through OSU. This fellowship provides summer salary support and will allow Lehman to complete her independent research project in Summer 2024. Two graduate students (Aniket Banerjee and Urvashi Verma) also led efforts to develop mathematical models. They have met with Dr. Margaret Lewis on a bi-weekly basis, so as to understand the ecological and entomological features of the various objectives, to model them accurately, in mathematical models. This has greatly benefitted their interdisciplinary training. They have met regularly with Dr. Rana Parshad, to fine tune the modeling nuances, as part of their PhD training. How have the results been disseminated to communities of interest?We have presented our research results at regional, national, and international scientific conferences, including the Entomological Society of America North-Central Branch Annual Meeting (invited talk, April 2023, Oklahoma City, OK), the Society of Industrial and Applied Mathematics sectional meeting (3 talks on the population dynamics of aphids under abiotic stresses, Lincoln, NE), the Entomological Society of America Annual National Meeting (November 2023, Vancouver BC), and the National Meeting for the American Chemical Society (invited talk, August 2023, San Francisco, CA). Additional, project results were also shared at the 2023 Climate Smart Conference, an extension meeting hosted by the Ohio State University that attracted a diverse stakeholder audience, including growers, extension agents, industry representations, and university researchers. Results will also be presented at additional scientific conferences during the upcoming year, including 4 anticipated talks at the Midwest mathematical Biology Conference (May2024, La Crosse, WI) and the Society of Industrial and Applied Mathematics national meeting (June 2024, Portland, OR). What do you plan to do during the next reporting period to accomplish the goals? Finish collecting and analyzing life table data and prepare publication Identify a molecular marker for differentiating between soybean aphid biotypes using RadSeq. Use marker to finish processing mixed soybean aphid mesocosm samples (Objective 3) Conduct laboratory assays to quantify flooding stress impacts on parasitoid preference for soybeans aphids and parasitoid fitness. Collect aphid samples for biochemical analyses to quantify flooding stress impacts on aphids as a host for parasitoids. Begin analyzing samples for quantities of key nutrients, including carbohydrates, proteins, and lipids. Submit modeling manuscripts for publication. Begin to analyze and simulate models with 1) parasitoid biocontrol 2) drift and dispersal of pests between soybean plants due to flooding 3) non-linear differential fitness models for virulent and avirulent aphids.
Impacts
What was accomplished under these goals?
In Fall 2023, we conducted laboratory mesocosm assays to quantify the impact of flooding stress on virulent and avirulent soybean aphid populations. These assays were conducted using two soybean varieties, an aphid-susceptible soybean variety and a near isoline soybean variety that was bred to express Rag1+2 aphid resistance genes. For each soybean variety, plants were either flooded continuously for 10 days or held under optimal water conditions and infested with either 8 virulent or 8 avirulent soybean aphid adults. Total aphid populations were quantified after 10 days of infestation. Flooding decreased avirulent aphid population densities by 28% and 44% on susceptible and Rag1+2 soybean varieties respectively, but it had not impact on virulent aphid populations. These results are consistent with our hypothesis that flooding stress in soybeans only has a negative impact on avirulent soybean aphid populations. This phenotypic data was incorporated into a manuscript that examines flooding impacts on the soybean aphid transcriptomic; the manuscript was submitted to the journal Molecular Ecology in December 2023 and is currently under review. This data has also been used to guide the development of mathematical models that quantify flooding impacts on aphid population dynamics (Objective 4). We began collecting samples for laboratory mesocosm assays with mixed virulent and avirulent aphid populations (Objective 3); these assays will allow us to test how water stress impacts the spread of virulence within an aphid population. In these assays, flooded or optimally watered soybean plants are infested with a mix of four virulent and four avirulent soybean aphid adults; after 10 days, we count the total number of aphids present on each plant and randomly sample 50 aphids, placing each aphid into individual PCR tubes for subsequent DNA extraction and molecular determination of aphid biotype. Aphid samples are currently being stored in a -20C freezer; we are currently working to develop a molecular marker that will allow us to distinguish between biotypes using a PCR or restriction enzyme digest based assay. Once those markers are developed, we will be able to process our freezer aphid samples, allowing us to determine the proportion of virulent and avirulent aphids present in a population under flooding and optimal water conditions. In January 2024, we began conducting life table experiments to compare the effect of water stress on virulent and avirulent soybean aphid population demographics (Objective 1). Because we observed similar responses to flooding regardless of soybean variety, life table experiments were only conducted using susceptible soybean. This reduced the number of treatments and has allowed for more robust replication. We have completed an estimated 20 - 25 replicates to date, with specific replication numbers varying between treatments (any experimental unit that had an aphid escape from the clip cage was excluded). In these life table assays, VC soybean plants were subjected to optimal water conditions or water stress conditions (seven days of continuous flooding followed by mild drought conditions); on each plant, neonate aphid nymphs were confined to individual leaves using clip cages. Aphids were checked daily, and we recorded survival, molting (as a measure of development), and daily nymph production. As the plants grew, aphids and clip cages were moved to newly emerged trifoliate. We anticipate completing all data collection and analysis by the end of summer 2024. We are currently developing and refining mathematical models that predict quantify water stress impacts on virulent and avirulent soybean aphid population dynamics. The classical boom-bust models (with one peak) that are commonly used to replicate/predict aphid population dynamics may not be accurate under global climate change, because abiotic factors could lead to more than one population peak in a growing season. We are therefore investigating models that have multiple peaks, including a basic one species model that uses a variable, time-dependent carrying capacity to replicate flooding stress impacts on aphid population dynamics. Issues with population explosion were identified in this model, so we are now investigating alternate models to submit a comprehensive manuscript for publication. A preprint detailing some of this work and has been submitted (https://doi.org/10.48550/arXiv.2310.03058). Additional modeling efforts have consider pests and beneficial insect dispersal into agricultural cropping fields. A preprint detailing this work has been submitted (https://doi.org/10.48550/arXiv.2310.17003), and is being fine tuned for a journal submission. We are currently investigating the possibility of extending these models to the soybean - soybean aphid system, considering the role that high amounts of rainfall and flooding might play in aphid dispersal.
Publications
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