NE2001: Harnessing Chemical Ecology to Address Agricultural Pest and Pollinator Priorities

(Multistate Research Project)

Status: Active

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SAES-422 Reports

Annual/Termination Reports:

[04/19/2021] [05/18/2022] [01/08/2024]

Date of Annual Report: 04/19/2021

Report Information

Annual Meeting Dates: 02/08/2021 - 02/10/2021
Period the Report Covers: 01/01/2020 - 01/01/2021

Participants

• Lynn Adler, University of Massachusetts Amherst
• Andrei Alyokhin, University of Maine
• Anurag Agrawal, Cornell
• Tom Baker, Penn State
• Yolanda Chen, University of Vermont
• Camila Filgueiras, Cornell
• Kelli Hoover, Penn State
• Rick Karban, UC Davis
• Erica Kistner Thomas, NIFA
• Greg Loeb, Cornell
• Scott McArt, Cornell
• Esther Ngumbi, University of Illinois
• Jan Nyrop, Cornell
• Cesar Rodriguez-Saona, Rutgers
• Jennifer Thaler, Cornell
• Rachel Vannette, UC Davis
• Denis Willett, Cornell
• Keyan Zhu-Salzman, Texas A&M

Participants Attachment:

NE2001 MultiState Meeting 2020.pdf

Brief Summary of Minutes

The theme of this meeting was ‘Where the Rubber Meets the Road’, identifying ways chemical ecology as a discipline and the NE2001 group in particular can positively impact agricultural management over the next 3-5 years. Chemical Ecology is uniquely poised to positively impact pest and pollinator management across agricultural systems. While great strides in our fundamental understanding of chemical communication have been made over the past decades, putting this understanding into practice remains an ongoing priority.

To that end, the objectives of this meeting were to:

Discuss new research developments over the past year.

Identify areas where chemical ecology as discipline can have the most impact over the next 3-5 years.

Identify ways of collaborating to meet those goals.

On February 8, the group met to discuss research developments over the past year with individual presentations by many participants and a discussion from Dr. Kistner-Thomas from NIFA. These presentations are discussed in the Accomplishments section below.

On February 9, the group met to brainstorm and discuss objectives 2 and 3 – where chemical ecology can have the most impact and opportunities for collaboration. The goal of these conversations was to generate many ideas around these objectives based on the specialties and domain expertise of the members in our group.

On February 10, the group met to refine ideas generated on February and develop focus areas

Specifically, the group identified:

Areas of Impact:

Leverage Past Successes. Chemical ecology as a discipline has had notable successes in improving pest management over the last few decades ranging from implementations of mating disruption, to recruitment of natural enemies, stimulation of plant defenses, push-pull systems, and other implementations of attractants and repellents. Much basic research has been done in each of these areas, and bringing an applied focus to this work can bear fruit. In each of these use cases, some implementations work really well and others have little impact. We see great potential in understanding why certain strategies work across systems - identifying the specific factors that lead implementation strategies to succeed and to fail – then leveraging that knowledge for prescriptive and predictive practices that succeed broadly across a wide spectrum of agricultural systems.

Combined with this idea of leveraging past successes and understanding how these strategies succeed in specific settings is the opportunity to stack strategies to ensure success. We unanimously agree that combining chemical ecology control strategies has enormous potential for ensuring successful management and believe that there are opportunities for additive and even synergistic effects from combined strategies that could deliver substantial positive impacts of yields.

The perceived outcome of leverage our past successes would be the ability to make these strategies more robust and anti-fragile in order to deliver results to producers across systems and vastly different environments. More work is needed to understand these factors, limitations, potential, and any additive or synergistic effects of combined strategies. We believe that substantial research progress can be made in this area over the next 3-5 years and will deliver tremendous economic benefit.

Improved Pest Monitoring Ability. The ability to detect and monitor pest populations is a critical first step in management decision making. Knowing when a pest is present and where a pest is located enables precision targeting of intervention strategies to ensure productive yields. Chemical ecology as a discipline has historically delivered in this area and continues to see potential in using new technology to enhance grower decision making. Historically, the development of pheromone-based attractant lures has had an outsize impact in the ability of producers to detect and monitor pest populations over the course of the growing season.

The group sees great potential in building on that historical success in two ways. The first is the ability to develop and use non-pheromone-based attractants and lures both in conjunction with pheromone-based lures and independently to improve monitoring ability. Here, research is needed both in terms of developing these lures and in connecting catch with levels of economic damage. The second is the ability to use our knowledge of chemical ecology to build chemical detection systems – volatile sensors – that can detect pests and pathogens based on their volatile signatures in agricultural systems. Here research is needed to both continue developing these sensors and in identifying volatile signatures indicative of pest presence.

The outcome of this work would be the ability of producers to rapidly detect pest presence and monitor their development over the course of the season. We anticipate that this work would allow producers to detect pests earlier than is currently possible, detect and monitor pests to an extent greater than is currently possible and connect that information to decision making frameworks and levels of economic damage in a manner that is both precise and eminently useful. We expect that research development in this area will have outsize impact over the next 3-5 years. Specifically, we see tremendous opportunity to not only improve management through reducing extant pest problems, but also drastically reduce prophylactic and non-targeted management strategies.

Plant Signaling. Breakthroughs in our understanding of plant signaling, both within and between organisms have led our group to believe that there is the potential for revolutionary advancements in our ability to leverage our understanding in development of more effective management strategies. While we see great potential in this area, we recognize that there are large gaps in our basic understanding of how these systems work and the ramifications of manipulating these systems in an agricultural environment. Research aimed at addressing these gaps is a priority and our group estimates that such research with begin to have outsize impact on a larger time-frame over the coming decades. Our group is uniquely poised to address these challenges, however with collaborative research connecting all aspects of chemically-mediated plant-insect interactions.

As a general point of consensus from the group, the past work on this project has generated substantial amounts of basic research and some applied research into each of these areas more or less independently. The group sees great potential in working together to combine knowledge in the applied space to stack and layer advances in each of these areas for more impactful outcomes over the next 3-5 years.

Opportunities for Collaboration:

The group identified a critical opportunity for radical collaboration around leveraging past successes and evaluating them across systems. Given the diversity of systems in which we conduct research, we are uniquely positioned to conduct similar assays across environmental and cropping systems in order to arrive at an understanding at how and why certain approaches work consistently. Dr. Rodriguez-Saona has already initiated this work with a meta-analysis, landscape-wide assessment of factors influencing natural enemies, and a proposed framework for future studies.

Accomplishments

The group has continued building upon the work done in previous iterations of this project with a renewed focus on core objectives.  The focus of this meeting was in developing the core areas listed above.    Additionally, the Chemical Ecology Core Facility continues its work with a number of members and looks to continue expanding.  Scott McArt presented on the use of the facility and proposed plans for expansion.  Other work and accomplishments over the past year include:    <ul> <li>The novel use of knowledge of attractive behavior to control mushroom phorid fly from Tom Baker’s program.</li> <li>Advances in the behavioral manipulation of Spotted Wing Drosophila for improved applied management by Greg Loeb’s program</li> <li>Work from Rick Karban’s program on two of the big challenges in using volatile cues to induce plant resistance to herbivores by identifying what the biologically active cues are that plants use and understanding the selective pressures that have shaped those cues. Towards that end, we have been studying the volatile cues that are emitted by damaged sagebrush plants from populations that vary in the levels of herbivore damage that they experience. A recent paper by Kalske et al. (2019 Current Biology) predicted that populations that experience high levels of damage will converge on a limited number of cues that are perceived by most individuals while populations that experience low levels of damage will evolve diverse cues that are perceived by only kin. We tested this hypothesis using 15 populations of sagebrush in California and Nevada. Our results supported this hypothesis and provide insights into the constraints on the evolution of plant signals.</li> <li>Examination of the ability of the spotted lanternfly to sequester chemical defenses by Kelli Hoover’s program.</li> <li>How Aphids respond to potatoes infected by Dickeya by Andrei Aloykhin’s program.</li> <li>Work from Anurag Agrawal’s program on squash – insect pest interactions, examining the roles of breeding history and insect pheromones as a means to enhance control of the striped cucumber beetle - Acalymma vittatum. Previous work has shown that these beetles 1) have an aggregation pheromone, 2) are more attracted to zucchini and related domesticates (Cucurbita pepo pepo) compared to summer squash (an independent domesticate, Cucurbita pepo ovifera), and 3) are attracted to floral volatiles (which have been developed into commercially available lures). In our collaborative work with Michael Mazourek’s plant breeding lab, we have identified that beetle aggregation is reduced on p. ovifera by a plant volatile and emigration (rather than enhanced attraction or pheromone production on C. p. pepo). Additionally, we have found that Cucurbitacins are not playing a key role in squash - Acalymma interactions. Our current work is examining levels of squash attack by an emerging pest, the squash bug - Anasa tristis. The squash bug is often associated with beetle aggregation, and we have shown that bugs are specifically attracted to (or eavesdrop on) the beetle’s pheromone. This work has been replicated in NY, New Hampshire, and Maryland. Additionally, trials in multiple states indicate that the squash bug is more abundant on C. p. ovifera than C. p. pepo. Thus, the two squash domesticates have opposing resistance to these two pests. We are working to better understand how plant traits in the two domesticates and both floral and pheromone lures might be used to increase management of striped cucumber beetles and the emerging squash bug.</li> <li>Work from Denis Willett’s program on developing volatile sensors for early detection of pests and pathogens with successful case studies across cropping systems and post-harvest processing above and belowground without disturbing the crop or the soil. To this end, his lab has built a state of the art fully automated cloud-based robot-driven metabolomics and volatilomics facility at Cornell AgriTech. </li> <li>Improved behavioral manipulation of natural enemies with an emphasis on a systems approach to understanding by Cesar Rodriguez-Saona’s program.</li> <li>An improved understanding of how sub-lethal imidacloprid exposure alters methylation in Colorado potato beetle with implications for population management.</li> <li>Work from Jennifer Thaler’s group on non-lethal indirect chemically mediated predatory effects.</li> </ul>

Publications

Adler LS, Fowler AE, Malfi RL, Anderson PR, Coppinger LM, Deneen PM, Lopez S, Irwin RE, Farrell IW, Stevenson PC. Assessing chemical mechanisms underlying the effects of sunflower pollen on a gut pathogen in bumble bees. Journal of chemical ecology. 2020 Mar 23:1-0.   Adler LS, Irwin RE, McArt SH, Vannette RL. Floral traits affecting the transmission of beneficial and pathogenic pollinator-associated microbes. Current Opinion in Insect Science. 2020 Aug 28.   Aflitto NC, Thaler JS. Predator pheromone elicits a temporally dependent non‐consumptive effect in prey. Ecological Entomology. 2020 Oct;45(5):1190-9.   Benevenuto RF, Seldal T, Moe SR, Rodriguez-Saona C, Hegland SJ. Neighborhood effects of herbivore-induced plant resistance vary along an elevational gradient. Frontiers in Ecology and Evolution. 2020 May 8;8:117.   Brevik K, Bueno EM, McKay S, Schoville SD, Chen YH. Insecticide exposure affects intergenerational patterns of DNA methylation in the Colorado potato beetle, Leptinotarsa decemlineata. Evolutionary Applications. 2020 Nov 25.   Brochu KK, van Dyke MT, Milano NJ, Petersen JD, McArt SH, Nault BA, Kessler A, Danforth BN. Pollen defenses negatively impact foraging and fitness in a generalist bee (Bombus impatiens: Apidae). Scientific reports. 2020 Feb 20;10(1):1-2.   Brzozowski LJ, Gore MA, Agrawal AA, Mazourek M. Divergence of defensive cucurbitacins in independent Cucurbita pepo domestication events leads to differences in specialist herbivore preference. Plant, Cell & Environment. 2020 Nov;43(11):2812-25.   Brzozowski LJ, Gardner J, Hoffmann MP, Kessler A, Agrawal AA, Mazourek M. Attack and aggregation of a major squash pest: Parsing the role of plant chemistry and beetle pheromones across spatial scales. Journal of Applied Ecology. 2020 Aug;57(8):1442-51.   Cha DH, Roh GH, Hesler SP, Wallingford A, Stockton DG, Park SK, Loeb GM. 2‐Pentylfuran: a novel repellent of Drosophila suzukii. Pest Management Science. 2020 Nov 24.   Chen J, Webb J, Shariati K, Guo S, Montclare JK, McArt S, Ma M. Pollen-mimicking, enzyme-loaded microparticles to reduce organophosphate toxicity in managed pollinators. Cheng WN, Zhang YD, Liu W, Li GW, Zhu‐Salzman K. Molecular and functional characterization of three odorant‐binding proteins from the wheat blossom midge, Sitodiplosis mosellana. Insect science. 2020 Aug;27(4):721-34.   Crandall SG, Gold KM, Jiménez-Gasco MD, Filgueiras CC, Willett DS. A multi-omics approach to solving problems in plant disease ecology. Plos one. 2020 Sep 22;15(9):e0237975.   Crowley-Gall A, Rering CR, Rudolph AB, Vannette RL, Beck JJ. Volatile microbial semiochemicals and insect perception at flowers. Current Opinion in Insect Science. 2020 Oct 20.   Grof-Tisza P, Karban R, Pan VS, Blande JD. Assessing plant-to-plant communication and induced resistance in sagebrush using the sagebrush specialist Trirhabda pilosa. Arthropod-Plant Interactions. 2020 Mar 12:1-6.   Grout TA, Koenig PA, Kapuvari JK, McArt SH. Neonicotinoid Insecticides in New York State.   Guo H, Zhang Y, Tong J, Ge P, Wang Q, Zhao Z, Zhu-Salzman K, Hogenhout SA, Ge F, Sun Y. An aphid-secreted salivary protease activates plant defense in Phloem. Current Biology. 2020 Dec 21;30(24):4826-36.   Hodgdon EA, Hallett RH, Heal JD, Swan AE, Chen YH. Synthetic pheromone exposure increases calling and reduces subsequent mating in female Contarinia nasturtii (Diptera: Cecidomyiidae). Pest Management Science. 2021 Jan;77(1):548-56.   Jones AG, Hoover K, Pearsons K, Tooker JF, Felton GW. Potential Impacts of Translocation of Neonicotinoid Insecticides to Cotton (Gossypium hirsutum (Malvales: Malvaceae)) Extrafloral Nectar on Parasitoids. Environmental entomology. 2020 Feb 17;49(1):159-68.   Karban R, Yang LH. Feeding and damage‐induced volatile cues make beetles disperse and produce a more even distribution of damage for sagebrush. Journal of Animal Ecology. 2020 Sep;89(9):2056-62.   Karban R. The ecology and evolution of induced responses to herbivory and how plants perceive risk. Ecological Entomology. 2020 Feb;45(1):1-9.   Mirzaei M, Züst T, Younkin GC, Hastings AP, Alani ML, Agrawal AA, Jander G. Less Is More: A Mutation in the Chemical Defense Pathway of Erysimum cheiranthoides (Brassicaceae) Reduces Total Cardenolide Abundance but Increases Resistance to Insect Herbivores. Journal of Chemical Ecology. 2020 Dec;46(11):1131-43.   Ngumbi EN, Hanks LM, Suarez AV, Millar JG, Berenbaum MR. Factors associated with variation in cuticular hydrocarbon profiles in the navel orangeworm, Amyelois transitella (Lepidoptera: Pyralidae). Journal of chemical ecology. 2020 Jan;46(1):40-7.   Pereira RV, Filgueiras CC, Willett DS, Peñaflor MF. Sight unseen: Belowground feeding influences the distribution of an aboveground herbivore. Ecosphere. 2020 Sep;11(9):e03163.   Rering CC, Vannette RL, Schaeffer RN, Beck JJ. Microbial co-occurrence in floral nectar affects metabolites and attractiveness to a generalist pollinator. Journal of chemical ecology. 2020 Aug;46(8):659-67.   Rodriguez-Saona C, Urbaneja-Bernat P, Salamanca J, Garzón-Tovar V. Interactive Effects of an Herbivore-Induced Plant Volatile and Color on an Insect Community in Cranberry. Insects. 2020 Aug;11(8):524.   Rodriguez‐Saona C, Alborn HT, Oehlschlager C, Calvo C, Kyryczenko‐Roth V, Tewari S, Sylvia MM, Averill AL. Fine‐tuning the composition of the cranberry weevil (Coleoptera: Curculionidae) aggregation pheromone. Journal of Applied Entomology. 2020 Jun;144(5):417-21.   Ugine TA, Thaler JS. Insect predator odors protect herbivore from fungal infection. Biological Control. 2020 Apr 1;143:104186.   Urbaneja-Bernat P, Waller T, Rodriguez-Saona C. Repellent, oviposition-deterrent, and insecticidal activity of the fungal pathogen Colletotrichum fioriniae on Drosophila suzukii (Diptera: Drosophilidae) in highbush blueberries. Scientific reports. 2020 Sep 2;10(1):1-9.   Uyi O, Keller JA, Johnson A, Long D, Walsh B, Hoover K. Spotted Lanternfly (Hemiptera: Fulgoridae) can complete development and reproduce without access to the preferred host, Ailanthus altissima. Environmental entomology. 2020 Oct;49(5):1185-90.   Vannette RL. The floral microbiome: Plant, pollinator, and microbial perspectives. Annual Review of Ecology, Evolution, and Systematics. 2020 Nov 2;51:363-86.   Villalona E, Ezray BD, Laveaga E, Agrawal AA, Ali JG, Hines HM. The role of toxic nectar secondary compounds in driving differential bumble bee preferences for milkweed flowers. Oecologia. 2020 Jul;193(3):619-30.   Wanner KW, Moore K, Wei J, Herdlicka BC, Linn CE, Baker TC. Pheromone Odorant Receptor Responses Reveal the Presence of a Cryptic, Redundant Sex Pheromone Component in the European Corn Borer, Ostrinia nubilalis. Journal of Chemical Ecology. 2020 Jul;46(7):567-80.   Willett DS, Filgueiras CC, Benda ND, Zhang J, Kenworthy KE. Sting nematodes modify metabolomic profiles of host plants. Scientific reports. 2020 Feb 10;10(1):1-0.   Wolfin MS, Chilson III RR, Thrall J, Liu Y, Volo S, Cha DH, Loeb GM, Linn Jr CE. Habitat cues synergize to elicit chemically mediated landing behavior in a specialist phytophagous insect, the grape berry moth. Entomologia Experimentalis et Applicata. 2020 Dec;168(12):880-9.

Impact Statements

Despite COVID, the results of work on this project have been widely disseminated both through publications listed below and through presentations at national and international meetings by members of this project. Several post-doc, graduate, and undergraduate students have been trained through the work on this project, not just in terms of technical approaches to chemical ecology, but also in terms of asking and answering impactful questions and professional development.

Date of Annual Report: 05/18/2022

Report Information

Annual Meeting Dates: 01/10/2022 - 01/11/2022
Period the Report Covers: 01/01/2021 - 12/31/2021

Participants

Flor Aceveda, Penn State;
Lynn Adler, University of Massachusetts Amherst ;
Anurag Agrawal, Cornell;
Seung-Joon Ahn, Mississippi State;
Jared Ali, Penn State;
Clare Casteel, Cornell University;
Yolanda Chen, University of Vermont;
Christophe Duplais, Cornell;
Sanford Eigenbrode, Idaho;
Gary Felton, Penn State;
Angel Helms, Texas A & M;
Sara Hermann, Penn State;
Kelli Hoover, Penn State;
Rick Karban, UC Davis;
Monica Kersch-Becker, Penn State;
Erica Kistner- Thomas, NIFA;
Greg Loeb, Cornell;
Scott McArt, Cornell;
Jan Nyrop, Cornell;
Katja Poveda, Cornell University;
Tanya Renner, Penn State;
Monique Rivera, Cornell;
Chris Roh, Cornell;
Cesar Rodriguez-Saona, Rutgers;
Michael Stout, Louisiana State;
Jennifer Thaler, Cornell;
John Tooker, Penn State;
Susan Whitehead, Virginia Tech

Brief Summary of Minutes

This meeting had two major goals. The first was to introduce the group to the many new members and hear about current research. The second was to make concrete plans for group projects. Since the inception of this multistate project a goal has been to leverage our geographic breadth, breadth of approaches, and shared goals to work together to positively affect pest and pollinator management. During the previous annual meeting, we discussed general areas for group projects where participants thought we could be successful in translating our fundamental understanding of chemical communication into practice for pest and pollinator management. This year, a major goal was to develop concrete projects with applied potential that we could work on together.

To that end, the objectives of this meeting were to:

Discuss new research developments over the past year, in particular introducing new members.

Discuss four project ideas and measure the group’s interest in pursuing. Identify ways of collaborating to meet those goals.

On January 10, the group met to discuss research developments over the past year with individual presentations by many participants. These presentations are discussed in the Accomplishments section below. In the afternoon, we “pitched” the ideas for Group projects. The Group project ideas are also discussed in the Accomplishment section below.

On January 11, the group had an update and discussion with Dr. Kistner-Thomas from NIFA. We then delved deeper into and modified the four Group projects and a new idea for the group that emerged on the first day.

Accomplishments

Accomplishments: Short term outcomes: Building Opportunities for Collaboration:            Building on the areas of impact delineated at the last multistate meeting, several members of the group developed several areas with great potential to have applied impact over the next 3-5 years if given a concerted group effort. These projects were written up for all group members to consider before the meeting and formed the basis for much discussion during the meeting. The group identified a critical opportunity for radical collaboration around leveraging past successes and evaluating them across systems.  Given the diversity of systems in which we conduct research, we are uniquely positioned to conduct similar assays across environmental and cropping systems in order to arrive at an understanding at how and why certain approaches work consistently.  Four Group Projects <ol> <li>Predalure—a group experiment to evaluate the potential for using herbivore-induced plant volatiles to attract the natural enemies of herbivores. Methyl salicylate has been found to be attractive to natural enemies in many systems and is marketed under the tradename PredaLure (winter green oil—methyl salicylate). However, it is not known how different groups of natural enemies will respond to methyl salicylate in different crops and different locations. Cesar Rodriguez-Saona and his postdoc Patricia Prade (Rutgers) are spearheading this project to test this product in multiple crops and multiple states (New Jersey, New York, Pennsylvania, Virginia). We will also use this as an opportunity to train students and develop a cohort of undergraduate students across states in chemical ecology by involving them in group project meetings.</li> </ol>   <ol start="2"> <li>Synergisms in chemical ecology approaches—this group project will be a literature review on the success of chemical ecology based techniques when used alone and in combination with other approaches. Semiochemical mediated pest management relies on an IPM approach of combining multiple tactics and yet we do not have a solid understanding of how different strategies can be combined to maximize their effect. This project will explore the underlying mechanisms of how multiple stresses interact so we can layer and combine multiple mechanisms of action. We will consider these five areas of chemical ecology application to pest management Pheromones: attraction and mating disruption, attract and kill; Host plant resistance: passive and induced, the basis for many other of the mechanisms; Crop rotation: understanding the mechanisms fundamental; Intercropping: associational resistance mechanisms; Indirect defenses: fear factor, induced volatiles, retention in habitat, spatial patterns. For each of these categories, we will elaborate on the hypothesized mechanisms and alternatives. A desired outcome would be to predict which would act synergistically, additively or tradeoff. Would also like to highlight concrete next steps for research.</li> <li>Microbes in sustainable agriculture-- Clare Casteel Initiated discussions on a larger multi-state wide project on developing insect management tools based on soil-microbes and chemical ecology, with positive responses/interest from Dr. Kersch-Becker, Dr. Ali, and Dr. Wickings.</li> <li>Researchers working with companies trying to bring chemical ecology- based solutions to market noted the large regulatory hurdles encountered. Many of the chemical ecology based solutions are mixtures of compounds that are already approved for use in food, but are expensive to individually We will draft a letter to the EPA that identifies the ways the regulatory burden could be eased while maintaining safety standards.</li> </ol>   Outputs: Work and accomplishments over the past year include:  <ul> <li>The Poveda lab completed their project on the effects of exposure to pesticide residues on bee health, publishing one paper and submitting one more.</li> <li>Agrawal’s group completed a project on squash resistance to two major pests (squash bugs and striped cucumber beetles). They found opposing patterns of resistance two the 2 insects among the two major domesticates, and that the squash bug eavesdrops on the striped cucumber beetle's pheromone.</li> <li>Greg Loeb’s group tested the efficacy of candidate repellents for Drosophila suzukii in the lab and in raspberry field plots at different scales. They tested different methods for controlling release of volatile repellents under field conditions and measured ambient concentrations of candidate volatile repellent for Drosophila suzukii at different distances from release point and compared to infestation levels.</li> <li>Anh’s lab has identified multiple detoxification gene families from the genome/transcriptome analysis of different insects.</li> <li>Lynn Adler’s group analyzed data and prepared a manuscript relating land use and floral resources to bee diversity on sunflowers. They also prepared and published a manuscript showing that the effect of sunflower pollen on pathogen infection differs with bumble bee species. Finally, they conducted an experiment assessing drought effects on pesticides in pollen of three crops and sent pollen samples for pesticide analysis.</li> <li>Rachel Vannette’s lab finalized publication of work describing microbial suppression of floral pathogens and effects on honey bee feeding and are continuing to investigate the effects secondary chemicals in nectar on microbial growth and pollinator preference.</li> <li>Hilary Sandler conducted four field trials at UMass Cranberry Station evaluating a total of 13 novel compounds/regimes (including FRAC Group M1,7,19 and pre-mix combinations of 9&12, 7&12, 5 biocontrol/microbial formulations) in comparison with Grower Standards and non-sprayed control for their effect on cranberry fruit rot, yield and fruit quality parameters of interest.</li> <li>Clare Casteel initiated a new project on the role of soil microbiomes and farmer practices that mediate foliar defense induction in dry bean and other crops. They collected soil and plant tissue from a full factorial experiment with diverse cover crop regimes in the field from two regions in New York including soil samples from ~85 organic farmers in New York.</li> <li>John Losey’s lab initiated a new project to look at the role of carrot plant volatiles and floral and foliar resources on the lady beetle attraction and retention. They collected data on the palatability of five different common carrot species and found that they are not consumed by any of the 3 lady beetle species we have tested to date. Additionally, we have sewn and grown two species of biennial carrot species (Queen Anne’s lace and poison hemlock) for use in laboratory and field studies planed for summer 2022 and 2023. Finally, they established colonies of five lady beetle species in five different genera to use in our experiments.</li> <li>Monica Kersch-Becker collected preliminary data on the effects of salicylate defenses in strengthening pest control in tomato plants.</li> <li>Keyan-Zhu demonstrated that resistance to aphids in CCA1-ox Abrabidopsis line is due to elevated basal indole glucosinolate production, and that the CCA population of the green peach aphid can adapt to CCA1-ox.</li> <li>Jennifer Thaler’s group collaborated with Hermann’s group to test the release of predator pheromones in grower fields as a way to reduce Colorado potato beetle damage in potato and eggplant.</li> </ul> Milestones: As a group, we met a major milestone by establishing four large group projects. Individual projects met their own milestones.

Publications

<table width="0"> <tbody> <tr> <td>  Ahn, S.-J., Marygold, S.J. 2021. The UDP-glycosyltransferase family in Drosophila melanogaster: Nomenclature update, gene expression and phylogenetic analysis. Frontiers in Physiology 12, 648481. </td> </tr> <tr> <td> Bernaola, L., Butterfield, T.S., T.H. Tai, and M.J. Stout. 2021. Epicuticular wax rice mutants show reduced resistance to the rice water weevil and fall armyworm. Environmental Entomology, doi: 10.1093/ee/nvab038. </td> </tr> <tr> <td> Brzozowski, L. J., Weber, D. C., Wallingford, A. K., Mazourek, M., & Agrawal, A. A. (2022). Trade-offs and synergies in management of two co-occurring specialist squash pests. Journal of Pest Science, 95(1), 327-338. </td> </tr> <tr> <td> Bueno, E. M., C. McIlhenny, and Y. H. Chen. Submitted. Cross tolerance to stress in insect pests: Implications for pest management in a changing climate. Pest Management Science. </td> </tr> <tr> <td> Cha, D.H., Roh, G.H., Hesler, S.P., Wallingford, A., Stockton, D.G., Park, S.K., and Loeb, G. 2020. 2-pentyyfuran: a novel repellent of Drosophila suzukii. Pest Management Science 77: 1757-1764. </td> </tr> <tr> <td> <a href="https://doi.org/10.1038/s43016-021-00282-0">Chen, J., J. Webb, K. Shariati, S. Guo, J. K. Montclare, S. H. McArt and M. Ma. 2021. Pollen-inspired enzymatic microparticles to reduce organophosphate toxicity in managed pollinators. Nature Food 2:339-347. </a> </td> </tr> <tr> <td> Crandall, S. G., Spychalla, J., Crouch, U., Acevedo, F. E., Naegele, R., & Miles, T.D. 2022. Rotting grapes don’t improve with age: cluster rot disease complexes, management, and future prospects. Plant Disease. https://doi.org/10.1094/PDIS-04-21-0695-FE </td> </tr> <tr> <td> Crowley-Gall, A., Trouillas, F., Nino, E. L., Schaeffer, R. N., Nouri, M. T., Crespo, M., & Vannette, R. 2021. Floral microbes suppress growth of Monilinia laxa with minimal effects on honey bee feeding. Plant Disease. </td> </tr> <tr> <td> Davidson-Lowe, E., & Ali, J. G. 2021. Herbivore-induced plant volatiles mediate behavioral interactions between a leaf-chewing and a phloem-feeding herbivore. Basic and Applied Ecology, 53, 39-48. </td> </tr> <tr> <td> Fowler AE, Giacomini JJ, Connon SJ, Irwin RE and LS Adler. 2022. Sunflower pollen reduces a gut pathogen in the model bee species, Bombus impatiens, but has weaker effects in three wild congeners. Proceedings of the Royal Society of London B 289: 20211909. https://doi.org/10.1098/rspb.2021.1909 </td> </tr> <tr> <td> Grof-Tisza, P., R. Karban, M. U. Rasheed, A. Saunier, and J. D. Blande. 2021. Risk of herbivory negatively correlates with the diversity of volatile emissions involved in plant communication. Proceedings of the Royal Society B 288:20211790. </td> </tr> <tr> <td> Hauri, K.C., A.E. Glassmire, and W.C. Wetzel. 2021. Chemical diversity rather than cultivar diversity predicts natural enemy control of herbivore pests. Ecological Applications 31: e02289. </td> </tr> <tr> <td> Ji, R., J. Lei, I.W. Chen, W. Sang, S. Yang, J. Fang and K. Zhu-Salzman (2021) Cytochrome P450s CYP380C6 and CYP380C9 in green peach aphid facilitate its adaptation to indole glucosinolate-mediated plant defense. Pest Management Science 77: 148–158 </td> </tr> <tr> <td> Mason, C.M., M. Peiffer, A. St. Clair, K. Hoover and G.W. Felton 2021. Concerted impacts of antiherbivore defenses and opportunistic Serratia pathogens on the fall armyworm (Spodoptera frugiperda). Oecologia <a href="https://doi.org/10.1007/s00442-021-05072-w">https://doi.org/10.1007/s00442-021-05072-w</a>. Mason, C.J., Felton, Hoover. 2021. Effects of maize (Zea mays) genotypes and microbial sources in shaping fall armyworm (Spodoptera frugiperda) gut bacterial communities. Sci. Reports https://doi.org/10.1038/s41598-021-83497-2. Mason, C.J., K. Rubert-Nason, D. Long, R.L. Lindroth, J. Shi, and K. Hoover. 2021. Salicinoid phenolics reduce adult Anoplophora glabripennis (Cerambicidae: Lamiinae) feeding and egg production. Arthropod-Plant Interactions 15(1): 127-136. </td> </tr> <tr> <td> <a href="https://doi.org/10.3389/fevo.2021.813455">Piñero, J.C., Godoy-Hernandez, H., Giri, A., and Wen, X. 2022. Sodium chloride added to diluted Concord grape juice prior to fermentation results in a highly attractive bait for Drosophila suzukii (Diptera: Drosophilidae). Frontiers in Ecology and Evolution 9:813455. </a><a href="https://doi.org/10.3389/fevo.2021.813455">https://doi.org/10.3389/fevo.2021.813455</a>. </td> </tr> <tr> <td> Samuel Pallis, Andrei Alyokhin, Brian Manley, Thais B. Rodrigues, Aaron Buzza, Ethann Barnes, and Kenneth Narva. 2022. Toxicity of a Novel dsRNA-based Insecticide to the Colorado Potato Beetle in Laboratory and Field Trials. Pest Management Science, in press. </td> </tr> <tr> <td> Stockton, D.G., Cha, D.H., and Loeb, G.M. 2021. Does habituation affect the efficacy of semiochemical ovisposition repellents developed against Drosophila suzukii? Environmental Entomologist 50 (6), 1322-1321, doi.org/10.1093/ee/nvab099. ; Stockton, D.G., Cha, D.H., and Loeb, G.M. 2021. The effect of Erwinia amylovora infection in apple saplings and fruit on the behavior of Delia platura (Diptera: Anthomyiidae). Environmental Entomology, doi: 10.1093/ee/nvaa153. </td> </tr> <tr> <td> Urbaneja-Bernat, P., Cloonan, K., Zhang, A., Salazar-Mendoza, P., and Rodriguez-Saona, C. 2021. Fruit volatiles mediate differential attraction of Drosophila suzukii to wild and cultivated blueberries. Journal of Pest Science 94: 1249–1263. doi: 10.1007/s10340-021-01332-z. </td> </tr> </tbody> </table>

Impact Statements

The results of work on this project have been widely disseminated both through publications listed below and through presentations at national and international meetings by members of this project. Several post-doc, graduate, and undergraduate students have been trained through the work on this project, not just in terms of technical approaches to chemical ecology, but also in terms of asking and answering impactful questions and professional development. We are delighted that the group continues to attract new investigators from a variety of institutions.

Date of Annual Report: 01/08/2024

Report Information

Annual Meeting Dates: 10/26/2023 - 10/28/2023
Period the Report Covers: 11/01/2022 - 11/30/2023

Participants

In-Person Members: Cesar Rodriguez-Saona (Rutgers), Rupesh Kariyat (U of Arkansas), Anurag Agrawal (Cornell), Chase Stratton (Delaware), Katja Poveda (Cornell), Jennifer Thaler (Cornell), Monica Kersch-Becker (Penn State), Keyan Zhu Salzman (Texas A&M), Seung-Joon Ahn (Mississippi State), Zain Syed (Kentucky)
In-Person Students and post-docs: Jack Collins, Beth Yoshimura Ferguson, Jae Kerstetter, Yahel Ben-Zvi, Haotian Liu, Amanda Quadrel
Virtual Members and Postdoc: Yolanda Chen (Univ. of Vermont), Andre Kessler (Cornell), Blair Siegfried (Penn State), Hany Dweck (Ag station, Connecticut), Kelli Hoover (Penn State), Leela Uppala (Univ. of Mass Amherst), Andrei Alyokhin (Maine), Swayamjit Ray (Cornell), Binita Shrestha (Cornell), Greg Loeb (Cornell), Sarah Hind (Univ. of Illinois), Flor Acevedo (Penn State), Anjel Helms (Texas A&M), Erica Kistner Thomas (NIFA national program leader), Todd Ugine (Cornell)

Brief Summary of Minutes

Brief summary of minutes of annual meeting:

The meeting had two primary objectives. The first was to introduce the group with new members and gain insights into ongoing research. The second was to formulate specific plans for collaborative group projects. Since the beginning of our multistate project, our aim has been to leverage our geographic diversity, a variety of approaches, and shared goals to collectively impact pest and pollinator management positively. During the previous annual meeting, we identified broad areas for potential group projects where participants believed we could successfully translate our fundamental understanding of chemical communication into practical applications for pest and pollinator management. This year, a key focus was to update the members on these projects and explore new projects with applied potential that we could collaboratively pursue.

To that end, the objectives of this meeting were to:

Provide updates on the multistate Hatch project and NIFA funding sources.

Discuss new research developments over the past year, in particular introducing new members.

Discuss four project ideas and measure the group’s interest in pursuing. Identify ways of collaborating to meet those goals.

On October 27, 2023, the group met to discuss research developments over the past year with individual presentations by 12 participants. These presentations are discussed in the Accomplishments section below. In the afternoon, we provided updates of ongoing Group projects and discussed ideas for new projects. The Group project ideas are also discussed in the Accomplishment section below.

At the meeting, the group had an update on the multistate Hatch project by our administrative advisor Dr. Blair Siegfried and had an update and discussion with Erica Kistner-Thomas, National Program Leader from NIFA. We then discussed four Group projects.

Minutes Attachment:

chemical Ecology multistate report Oct 2023 meeting Jan 08 2024.pdf

Accomplishments

Short term outcomes: Building Opportunities for Collaboration: Building on the impact areas discussed during the previous multistate meeting, several group members have identified promising areas with significant applied potential over the next 3-5 years. These proposed projects were presented to the group and sparked extensive discussion during the meeting. Recognizing a critical opportunity for collaboration, the group aims to leverage past successes and evaluate their applicability across diverse systems. Given the variety of systems in which we conduct research, we are uniquely positioned to perform similar assays across different environmental and cropping systems, allowing us to gain a comprehensive understanding of how and why certain approaches consistently yield positive results. Four Group Projects <ol> <li>Opinion paper—the group discussed writing an opinion paper on the challenges facing the registration of semiochemicals for pest control. For this, the group invited Dr. Agenor Mafra-Neto, CEO of ISCA technologies. During the discussion, Dr. Mafra-Neto highlighted the current pathways for registering semiochemicals and shed light on the difficulties his company encounters, particularly when registering products containing blends of compounds that lack tolerance exemptions. The primary goal of the opinion paper is to educate the public, academia, and government agencies on semiochemicals, their applications, the hurdles in the registration process, and suggest potential solutions.</li> </ol>   <ol start="2"> <li>Predalure—a Group project was initiated in 2022 and continued in 2023 to evaluate the potential for using herbivore-induced plant volatiles to attract the natural enemies of herbivores. Methyl salicylate has been found to be attractive to natural enemies in many systems and is marketed under the tradename PredaLure (winter green oil—methyl salicylate). However, it is not known how different groups of natural enemies will respond to methyl salicylate in different crops and different locations. Cesar Rodriguez-Saona and his postdoc Patricia Prade (Rutgers) led this project to test PredaLure in multiple crops and multiple states (New Jersey, New York, Pennsylvania, Virginia). This project provided an opportunity to train students across states in chemical ecology by involving them in field research and group project meetings.</li> </ol>   <ol start="3"> <li>Meta-analysis on HIPVs—this group project led by Cesar Rodriguez-Saona and Sara Hermann will analyze data from peer-reviewed papers on the response of natural enemies of herbivores to synthetic herbivore-induced plant volatiles (HIPVs) in the field. While HIPVs have been employed for decades to attract natural enemies, their response may vary across different crops. Utilizing data from published papers, this project seeks to investigate and understand the diverse responses of natural enemies to HIPVs in the field. The ultimate goal is to predict how natural enemies react to HIPVs and identify key areas for future research.</li> </ol>   <ol start="4"> <li>Context of management strategies—Jennifer Thaler led discussions on the impact of various environmental conditions, such as soil composition, on management strategies like host-plant resistance.</li> </ol>   Outputs: Work and accomplishments over the past year include:  <ul> <li>Agrawal’s group have been studying striped cucumber beetle and squash bugs to examine joint management possibilities via chemical ecology and breeding. In particular, they have been studying their pheromones as well as plant resistance in the descendants of the two domestication events of Cucurbita pepo. Squash bugs exploit the pheromone of striped cucumber beetle for host choice and this has implications for management: while there are trade-offs in varietal preference based on the two domesticates, synergistic trapping of both pests may be possible (via shared use of pheromone cues).</li> <li>Kessler’s lab demonstrated in a maize intercropping system that chemical signals from neighboring plants as well as plant chemistry-mediated plant-soil feedbacks affect plant secondary metabolism and thus resistance to herbivores and biomass accumulation. Most importantly, plant-soil feedback affects plant secondary metabolism in fundamentally different ways than chemical signals from neighboring plants. In consequence, rotation cropping and intercropping of maize with legumes can have fundamentally different effects on plant metabolism and performance. Moreover, chemical elicitation effects differ with intercrop species.</li> <li>Syed’s lab is working on chemosensory basis of host/mate finding and avoidance/repellence. They just submitted a review of the concepts of attraction and repulsion in ticks. The lab continues to focus on researching spotted-wing drosophila (SWD) oviposition.</li> <li>Dweck’s lab is deciphering how spotted lanternfly (SLF), an invasive polyphagous planthopper in North America, engages with its environment is a pressing issue with fundamental biological significance and economic importance. This interaction primarily depends on olfaction. However, the cellular basis of olfaction in SLF remains elusive. The lab is identifying new odorants that may be useful for managing this serious pest.</li> <li>Karban’s lab continues to examine the mechanisms and consequences of volatile communication leading to induced resistance in Artemisia. They also conducted experiments examining the potential role of trichomes in communication in tomato and examined petal shading as a response to heat stress.</li> <li>Hoover’s lab is investigating whether sequestration of toxin from tree of heaven by the SLF affects predator feeding preference.</li> </ul> <ul> <li>Thaler’s lab is studying the non-consumptive effects of predators on herbivores and their potential use in agriculture. They are using the aggregation pheromone of stinkbug predator to reduce number of Colorado potato beetles and their damage and to increase tuber yield.</li> <li>Rodriguez-Saona’s lab is studying the effects of domestication on plant guttation and tri-trophic interactions. They are also studying the repellent effects of volatiles from anthracnose-infected fruits on SWD.</li> </ul> <ul> <li>McArt’s lab found that wax in NYS honey bee colonies contains 17 pesticides, on average, and some of these pesticides are known to synergize with each other. They also assessed how bees are exposed to pesticides in orchards and in this process found that most species of wild bees spill over from adjacent forest habitats to conduct crop pollination. When they placed experimental bumble bee colonies in orchards, they also found that they can function as ecological traps for wild nest-searching queens. This publication prompted rapid industry change in queen excluder practices for all outdoor hives sold in the USA.</li> <li>Loeb’s lab continued research on discovery and development of repellents for SWD including large scale field testing of 2-pentylfuran (2pf) in fall raspberries, including impacts on beneficial arthropods. Also conducted lab bioassays on two other candidate repellents and began lab bioassays on specific mechanisms underlying repellency of 2pf. Conducted lab assessments of response of larval parasitoids of SWD to infested and uninfested fruit odors.</li> <li>Casteel’s lab identified the 16 most common soil management practices across 80+ organic farms in NY. Two of the most common practices were cover cropping and composting. Using lab and field experiments we found cereal rye and canola cover crops reduced pest damage and enhanced plant resistance through changes in the soil microbiome. We used this data to obtain funding from NIFA ORG on the impact of seed origin on resilience enhancing soil microbiomes.</li> <li>Vannette’s lab continued to examine how nectar chemistry influences microbial communities and attraction to pollinators. We conducted experiments comparing nectar chemistry and antimicrobial potential of 30+ plant species. We examined responses of 3 pollinator species to microbial colonization of nectar. We examined the role of hydrogen peroxide in antimicrobial defense of nectar.</li> <li>Losey’s lab collected volatiles from the flowers and foliage of several species of carrot plants (Queen Anne's lace, poison hemlock, and wild parsnip). They have separated out the volatiles using GC-MS and characterized their emissions using principal component analyses. They found that the flowers of the three plants have several compounds in common that are candidate attractants for predators. They are now testing these compounds singly and in combination for their attractiveness to lady beetles. Additionally, we have identified and annotated all of the chemoreceptors (ionotropic, gustatory, olfactory, etc.) from the genomes of several lady beetle species for downstream functional characterizations in attraction.</li> <li>The focus of Dr. Ahn’s lab is on insect-plant interactions using biochemical and molecular tools not only to understand host plant adaptation strategies of arthropod herbivores, but also to develop novel strategies for integrated pest management. They have established a CRISPR/Cas9 technique to edit the genomes of lepidopteran species, including soybean looper and corn earworm. A visual phenotypic marker gene was successfully knocked out to prove the concept of the technique. They are currently applying to edit detoxification genes to understand the molecular mechanism of host-plant adaptation.</li> <li>Keyan-Zhu’s lab is studying the genetic and molecular bases of insect-plant-environment interactions, using electron beam to control storage insect pests and insect-vectored diseases, uncovering the mechanism of insect tolerance to hypoxia, and exploiting the metabolic constraint in insects and manipulate plant sterol profiles to control herbivore insects.</li> <li>Stout’s group found that rice plants deficient in their ability to take up silicon from the soil were more susceptible to fall armyworm in greenhouse trials and to brown spot in field trials. Levels of some secondary metabolites were affected in mutants but the ability of mutant plants to respond to herbivory was not compromised. Two methods of coating rice seeds with solutions containing methyl jasmonate were evaluated in field trials but neither was as effective as seed soaking. Treatment of cotton seeds with methyl jasmonate imparted resistance in seedlings to thrips. They also characterized the spatial extent of induction of ipomeamarone (furnaoterpenoid) by sweetpotato weevil.</li> <li>Stratton’s lab contributed preliminary work on an electroantennography study testing whether SWD habituates to natural repellents. They were also able to establish plants at our field station. One of the species, Silphium integrifolium, has insecticidal compounds they are interested in testing. They also established the Cheminformatics/Bioinformatics Data Processing Unit where they are filling out chemical function dictionaries for high-throughput functional screening of plant chemicals.</li> <li>Alyokhin’s lab continued work on using RNAi for managing Colorado potato beetles. The first sprayable active ingredient based on dsRNA, ledprona, has been issued an experimental use permit for the 2023 growing season. They tested the effects of ledprona on olfactory responses of Colorado potato beetles.</li> <li>Kariyat’s lab is studying the chemical ecology of soybean- soybean looper interactions and rice-fall armyworm interactions.</li> <li>Chen’s lab optimized the protocols for histone extractions and quantification. We have generated helpful preliminary data on the relationship between insecticide dosage and histone modifications.</li> <li>Poveda’s lab performed growth chamber and field experiments to test the attraction of seedcorn maggot to different soil amendments. They found that soil amendments such as manure and decomposing organic matter are very attractive for seedcorn maggot.</li> <li>Duplais’ lab is starting a project to evaluate the effectiveness of pheromone traps for monitoring insect pests. They aged corn earworm and codling moth lures from different suppliers and quantified the amount of pheromone emitted and remaining in the dispenser after aging the lures from 1 to 4 weeks in the field. They establish a correlation between the amount of pheromone emitted and the number of catch. They are also studying the detoxification of tomato steroidal alkaloid in the cabbage lopper. They have identified the detoxification product, the quantity uptaken, and the time required to excrete it from the caterpillar's body. They showed the variation between a wild-type strain and a Bt-resistant strain.</li> <li>Adler’s lab is studying how sunflowers affect bee communities, parasite resistance and health in agroecosystems, and also intersections between abiotic conditions (drought), pesticide exposure and pathogen dynamics in the common eastern bumble bee.</li> <li>Helms’ lab is evaluating the impacts of introducing beneficial insect-killing nematodes for biological control and enhanced plant resistance to improve pest management in cucurbit crops. We are also characterizing chemically mediated interactions among plants and herbivores in a squash agroecosystem to better understand plant resistance and impacts on the herbivore community. </li> <li>Kersh-Becker’s lab focused on two key areas: (1) the impact of climate change on tritrophic interactions and (2) the effects of plant defenses on biological control. Their findings revealed that while drought can decrease pest numbers, it reduces the efficacy of biological control. Additionally, they found that salicylate defenses of plants enhance the biological control of aphids.</li> <li>Members of the UMass Cranberry Station (Sandler, Uppala, Mupambi) evaluated several coppers and biologicals products in 2022 and 2023 growing seasons SOLO and as part of fungicide regimes with a goal to develop an integrated cranberry fruit rot management program, identified fungicide regimes with coppers and biologicals that worked efficiently in reducing fruit rot, studied the fruit and soil microbiome of cranberry from wild and managed (conventional and organic) ecosystems through 16 S and ITS sequencing, and characterized the most prevalent cranberry fruit rot fungi from Massachusetts cranberry bogs using Multiplex PCR.</li> </ul> Milestones As a group, we met a major milestone by establishing four large group projects. Individual projects met their own milestones.

Publications

Publications Aflitto, N. Ugine, T, Dittmar, A, and J.S. Thaler. 2023. Semiochemical release and ontogenetic changes in a primary scent gland of Podisus maculiventris. J. Chemical Ecology https://doi.org/10.1007/s10886-023-01411-8 Babu, A., Rhodes, E.M., Rodriguez-Saona, C., Liburd, O.E., and Sial, A.A. 2023. Comparison of multimodal attract-and-kill formulations for managing Drosophila suzukii: behavioral and lethal effects. PLoS ONE 18(12): e0293587. doi: 10.1371/journal.pone.0293587. Bhavanam, S and M.J. Stout. 2022. Varietal resistance and chemical ecology of the rice stink bug, Oebalus pugnax, on rice, Oryza sativa. Plants 2022, 11(22), 3169; https://doi.org/10.3390/plants11223169 Bischoff, K., N. Baert, and S. H. McArt. 2023. Pesticide contamination of beeswax from 72 managed honeybee colonies in New York State. Journal of Veterinary Diagnostic Investigation 35:617-624. https://doi.org/10.1177/10406387231199098 Brzozowski, L.J., D.C. Weber, A.K. Wallingford, M. Mazourek, and A.A. Agrawal.  2022. Tradeoffs and synergies in management of two co-occurring specialist squash pests. Journal of Pest Science 95: 327–338. Bueno, E. M., C. McIlhenny, and Y. H. Chen. 2022. Cross-protection interactions in insect pests: Implications for pest management in a changing climate. Pest Management Science. https://onlinelibrary.wiley.com/doi/abs/10.1002/ps.7191 Caitlin, R., Quadrel, A., Urbaneja-Bernat, P., Beck, J.J., Ben-Zvi, Y., Khodadadi, F., Aćimović, S.G., and Rodriguez-Saona, C. 2023. Blueberries infected with the fungal pathogen Colletotrichum fioriniae release odors that repel Drosophila suzukii. Pest Management Science. doi: 10.1002/ps.7692 Cecala, Jacob M., and Rachel L. Vannette. Nontarget impacts of neonicotinoids on nectar-inhabiting microbes. bioRxiv (2023): 2023-11                            Chang, Y., J. Lei, A.E. Alvarez, T. Chappell, X. Tang, I.W. Chen, C. Penca, W.D. Bailey, S. Pillai, C. Tamborindeguy, Y. Du and K. Zhu-Salzman (2023) Electron beam irradiation reduces bacterial abundance and transmission by potato psyllids. Entomologia Generalis 43: 441-450.  Chen, J., X. Chen, M.J. Stout, and J.A. Davis. 2022. Belowground herbivory to sweetpotato by sweetpotato weevil (Coleoptera:Brentidae) alters population dynamics and probing behavior of aboveground herbivores. Journal of Economic Entomology 115: 1069-1075, https://doi.org/10.1093/jee/toac098. Chen, Y. H., Z. P. Cohen, E. M. Bueno, B. M. Christensen, and Sean D. Schoville. 2023. Rapid evolution of insecticide resistance in the Colorado potato beetle, Leptinotarsa decemlineata. Current Opinion in Insect Science 55: 101000. https://doi.org/10.1016/j.cois.2022.101000 Cohen, Z. P., Y. H. Chen, R. Groves, and S. D. Schoville. 2022. Evidence of hard-selective sweeps suggest independent adaptation to insecticides in Colorado potato beetle (Coleoptera: Chrysomelidae) populations. Evolutionary Applications 15(10): 1691-1705. https://onlinelibrary.wiley.com/doi/10.1111/eva.13498 Fabri-Lima, A.1, Aguirre, N.M.1, Grunseich, J.G.1, Carvalho, G.A., Helms, A.M., Peñaflor, M.F.G.V. (2023) Effects of neonicotinoid seed treatment on maize anti-herbivore defenses vary across plant genotypes. Journal of Pest Science, https://doi.org/10.1007/s10340-023-01641-5 Fowler AE, Kola EU and LS Adler 2023. The effect of sunflower pollen age and origin on pathogen infection in the common eastern bumble bee, Bombus impatiens (Apidae: Hymenoptera). Journal of Economic Entomology toad154, https://doi.org/10.1093/jee/toad154 Francis, Jacob S., Tobias G. Mueller, and Rachel L. Vannette. Intraspecific variation in realized dispersal probability and host quality shape nectar microbiomes. New Phytologist 240.3 (2023): 1233-1245. Gikonyo, M.W., Ahn, S.-J., Biondi, M., Fritzlar, F., Okamura, Y., Vogel, H., Köllner, T.G., Şen, I., Hernández-Teixidor, D., Lee, C.-F., Letsch, H., Beran, F. 2023. A radiation of Psylliodes flea beetles on Brassicaceae is associated with the evolution of specific detoxification enzymes. Evolution qpad197. https://doi.org/10.1093/evolut/qpad197 Grant, C., Saurabh, K., Hayward, A., Hunt, B.J., Troczka, B.J., Pym, A., Ahn, S.-J., Zeng, B., Gao, C., Leroux, A., Daum, E., Süess, P., Souza, D., Elias, J., Richard, H., Vontas, J., Roditakis, E., Bielza, P., Zimmer, C.T., Bass, C. 2023. Overexpression of the UDP-glycosyltransferase UGT34A23 confers resistance to the diamide insecticide chlorantraniliprole in the tomato leafminer, Tuta absoluta. Insect Biochemistry and Molecular Biology 159, 103983. He, L., I.W. Chen, Z. Zhang, W. Zheng, A. Sayadi, L. Wang, W. Sang, R. Ji, J. Lei, G. Arnqvist, C. Lei and K. Zhu-Salzman (2022) In silico promoter analysis and functional validation identify CmZFH, the co-regulator of hypoxia-responsive genes CmScylla and CmLPCAT. Insect Biochemistry and Molecular Biology 140, 103681.  Hoover, K., L. Iavorivska, E. K. Lavely, O. Uyi, B. Walsh, E. Swackhamer, and D. M. Eissenstat. 2023. Effects of long-term feeding by spotted lanternfly on ecophysiology of common hardwood host trees. Environ. Entomol. https://doi.org/10.1093/ee/nvad084. Isbilir, S., Catchot, B., Catchot, L., Musser, F.R., Ahn, S.‐J. 2023. Molecular characterization and expression patterns of a ryanodine receptor in soybean looper, Chrysodeixis includens. Archives of Insect Biochemistry and Physiology 114, e22047. Johnson, A., A. Cornell, and K. Hoover. 2023. Birds biting bad bugs: Using community science to identify endemic predators of spotted lanternfly (Lycorma delicatula) in North America. Bulletin of Entomological Research, 1–8. https://doi.org/10.1017/S0007485323000317. Kalske, A., Shiojiri, K., Uesugi, A., Sakata, Y., Morrell, K., and Kessler, A. (2019). Insect herbivory selects for volatile-mediated plant-plant communication. Curr. Biol. 29, 3128–3133.       Karban, R. and A. A. Agrawal. 2023. The distribution of species interactions. Quarterly Review of Biology 98:203-218 Karban, R., D. Rutkowski and N. A. Murray. 2023. Flowers that self-shade reduce heat stress and pollen limitation. American Journal of Botany 110:e16109. Labbé F, Abdeladhim M, Abrudan J, Araki AS, Araujo RN, Arensburger P, Benoit JB, Brazil RP, Bruno RV, Bueno da Silva Rivas G: Genomic analysis of two phlebotomine sand fly vectors of leishmania from the new and old World. PLoS neglected tropical diseases 2023, 17:e0010862. Lavely, E.K., L. Iavorivska, O. Uyi, E. Primka, J.  Harper, B. Walsh, D.M. Eissenstat, and K. Hoover.  2022. Impacts of short-term feeding by Lycorma delicatula on ecophysiology of hardwood trees in a common garden. Front. Insect Sci. https://doi.org/10.3389/finsc.2022.1080124. Lei, J., Y. Tan, F. List, R. Puckett, A.M. Tarone, E.L. Vargo and K. Zhu-Salzman (2022) Cloning and functional characterization of a dsRNA-degrading nuclease in the tawny crazy ant (Nylanderia fulva). Frontiers in Physiology 13:833652. doi: 10.3389/fphys.2022.833652.  Lingeman D, O'Dell K, Syed Z: Developing attractants and repellents for ticks: Promises and challenges Current Opinion in Insect Science 2023. List, F., A.M. Tarone, K. Zhu-Salzman and E.L. Vargo (2022) RNA meets toxicology: Efficacy indicators from the experimental design of RNAi studies for insect pest management. Pest Management Science 78: 3215-3225.  Littler A, Pandey P, O'Dell KL, Syed Z: Chemical Ecology of Oviposition Dynamics in Drosophila suzukii (Diptera: Drosophilidae). J Econ Entomol 2022, 115:1029-1035. Liu, Z., S. Hou, O. Rodrigues, P. Wang, D Luo, S. Munemasa, J. Lei, J. Liu, F.A. Ortiz-Morea, X. Wang, K. Nomura, C. Yin, H. Wang, W. Zhang, K. Zhu-Salzman, S.Y. He, P. He and L. Shan (2022) Phytocytokine signalling reopens stomata in plant immunity and water loss. Nature 605:332–339.  Mason, C. J., M. Peiffer, K. Hoover, and G. Felton. 2023. 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Impact Statements

The outcomes of this project have been extensively shared through the publications listed below, as well as presentations at both national and international meetings by project members. The impact extends beyond disseminating technical approaches to chemical ecology; numerous post-docs, graduate, and undergraduate students have received training in posing and addressing impactful questions and have undergone significant professional development. We are pleased to note that the group continues to attract new investigators from various institutions.