NE1501: Harnessing Chemical Ecology to Address Agricultural Pest and Pollinator Priorities

(Multistate Research Project)

Status: Inactive/Terminating

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Annual/Termination Reports:

[09/29/2017] [03/10/2018] [02/05/2019] [01/20/2020]

Date of Annual Report: 09/29/2017

Report Information

Annual Meeting Dates: 11/17/2016 - 11/18/2016
Period the Report Covers: 10/01/2016 - 09/30/2017

Participants

Yolanda Chen, University of Vermont, Burlington
Jennifer Thaler, Cornell University
Anurag Agrawal, Cornell University
Andre Kessler, Cornell University
Michael Mazourek, Cornell University
Scott McArt, Cornell University
John Tooker, Pennsylvania State University
Lynn Adler, University of Massachusstts Amherst
Susan Whitehead, Virginia Tech
Gregory Loeb, Cornell University
Kyle Wickings, Cornell University
Sanford Eigenbrode, University of Idaho
Katja Poveda, Cornell University
Cesar Rodriguez-Saona, Rutgers University
Ian Kaplan, Purdue University
Shadi Atallah, University of New Hampshire
Chris Gonzales, Northeastern IPM Center
Gary Felton, Pennsylvania State University
Jared Ali, Pennsylvania State University
Rachel Vannette, UC Davis.

Brief Summary of Minutes

The group met on November 18, 2016 on the Cornell campus in Ithaca, NY. We had 20 participants attending the meeting that was led and organized by Jennifer Thaler. Some of these participants had not joined the multistate group at that point and were interested in learning more about it. One important outcome is that all of the “external” participants are now part of our multistate group and are following up on the collaborations that they started during the meeting.

Since this was the first meeting of the group we dedicated half a day to talks designated to get to know the research interests of all participants. This was achieves by short 5 minute presentations of each participant that highlighted the areas of their research that were particularly relevant for this group.

The afternoon session was devoted to talking about potential future collaborations. We divided into thematic areas identified by the group as the most important areas that would be relevant for NYS agriculture and where chemical ecology could provide real solutions to current problems. Those thematic areas were:

Domestication effects on plant resistance, plant-herbivore, plant-pollinators and plant-natural enemy interactions

Multispecies interactions/interactions across tissues

Context dependency of chemically mediated interactions from metabolic interactions to communities and landscape effects

How to increase the adoption of chemical ecology tools by farmers and how to increase our communication with the public

Non-target effects of pesticides

Linking pollinator health to germplasm improvement.

The most important decisions that were made during this meeting, where:

that the next organizational meeting was going to be located again in Ithaca, NY, since the location has a strong chemical ecology core group and is interesting for most participants to visit.

that the chair of the Executive Committee for the next year was going to be Katja Poveda, the representative at large Andre Kessler and that Yolanda Chen would fulfill the role of secretary.

that for our next organizational meeting the goal was to include the participation of farmers, as we wanted to look into the potential of submitting a USDA OREI (Organic Agriculture Research and Extension Initiative) to use push-pull techniques in the Northeast to reduce pest pressure, enhance biological control and ideally also enhance pollination. We did not take any decisions on the specific crop, but thought of potato, in a diversified system with vegetables and small berries as an ideal systems to pursue.

Accomplishments

Outputs: The most significant outputs has been the writing of research proposal based on preliminary data gathered since the establishment of this multistate project. For example for the project focused on the control of herbivores of cucurbits, two new projects have been submitted (see below) and one has already been approved for funding. Also the first manuscripts have been submitted and even published during this time (for details see impact statement below). Most PI’s involved in this multistate have also disseminated their results at national conferences like the Ecological Society of America meeting and the Entomological Society of America meeting. PI’s have also interacted with farmers, and other stakeholders such a beekeepers and crop breeders, to start establishing means by which the performed research can be translated to tools and management strategies to protect pollinators, reduce pest pressure and increase yields. Our collaboration with the Northeast IPM center has also rendered us a piece in their newsletter (<a href="http://www.northeastipm.org/about-us/publications/ipm-insights/plants-have-natural-defense-systems/">http://www.northeastipm.org/about-us/publications/ipm-insights/plants-have-natural-defense-systems/</a>) that describes the objectives of this multistate and allows us to disseminate the importance of tools based on chemical ecology for more sustainable crop production. Activities: <ul> <li>Related with our first and second objective, the project focused on controlling herbivores of cucurbits (lead by Mike Mazourek, Cornell University) has developed assays for the highly sensitive quantification of cucurbitacins using SPE concentration and LC-MS. This technique is used for sampling squash seedlings that define different taxonomic groups including inter and intraspecific comparisons that differ in their degree of damage by striped cucumber beetles. No differences were found for true leaves although they are most conspicuously damaged plant tissue in the field and further they were below the detection thresholds of the herbivore. Cotelydon differences aligned with beetle preference and were within beetle detection thresholds. This group hypothesized that beetle preference in squash is not determined by cucurbitacin concentration. To test this hypothesis, they exposed young seedlings of highly preferred squash (golden zucchini) and compared damage to non-preferred squash seedlings (summer squash). Comparisons were performed with either cotyledon or true leaves removed. In each experiment the beetles preferred golden zucchini tissue over the corresponding tissue in summer squash. The group interpreted this to mean that beetle feeding preferences are determined by another factor, other than cucurbitacins. This group has also adapted high resolution carotenoid separation methods to our HPLC system and calibrated it with known standards. Experiments are underway to look at carotenoid accumulation in different plant tissues that also exhibit preference differences by striped cucumber beetles.</li> <li>Regarding our second objective (Define variability of chemically mediated interactions between pests, crops, and beneficial organisms in terms of plant chemistry, species interactions and landscape factors in the Northeast), one group lead by Jennifer Thaler and Katja Poveda started a project measuring the relationship between potato plants, Colorado potato beetles and their predators on organic farms in Central New York. These farms were chosen to reflect a gradient from low-levels of agriculture to high levels of agriculture in the surrounding landscape. Preliminary data indicate that herbivore responses to predators depend on the landscape complexity. Jennifer Thaler’s group also investigated the defensive responses of Colorado potato beetles to stink bug predators using a population of beetles from Ithaca, NY. They have found large decreases in feeding and growth of beetles when predators are present but not consuming beetles. Combining these results is an advance in understanding the causes of variation in the predator-prey interaction and will be helpful in designing biological control practices in the future.</li> <li>In the front of pollinator research Lynn Adler has been leading an effort to understand how pollinator populations can be supported based on the quality of the host plants. This past year, they discovered that the medicinal value of sunflower pollen extends to a wide range of sunflower cultivars, wild sunflower accessions, two other Helianthus congeners, and even two Solidago species, which are in the same family as sunflower but not very close relatives. This discovery suggests that a wide range of sunflower relatives may be beneficial to the common eastern bumble bee and useful for treating Crithidia infection.</li> <li>The group lead by Richard Karban in this past year has learned how to make more effective use of volatile communication to induce resistance against insect herbivores. Specifically, they have learned that variation in the nutritional quality of crops can reduce the efficiency and success of herbivores across many different species of plants and insects. They also identified important sources of variation in plant quality in their model system for plant communication, Artemisia tridentata. Individuals vary in the major chemicals that they emit when they are attacked or damaged. This chemotypic variation affects how effectively they respond to cues of damage. The effectiveness of communication also is affected by the geographic proximity of the source of volatile cue, suggesting that plant cues may exhibit geographic dialects.</li> <li>Anurag Agrawal’s groups has been investigating ways to aid to the conservation of non-target organisms such as the monarch butterfly to agricultural practices, specifically the use of herbicides. Specifically they are investigating the use of swallow-worts by monarch butterflies, which are used for oviposition but do not support caterpillars. In this project they are investigating the use of swallow-worts by monarchs, the chemical cues used by monarchs to recognize them, and the impacts of reduced milkweed availability due to herbicide usage on their preferences. Initial experiments showed reduced oviposition on swallow-wort in the presence of milkweed. Chemical analyses are currently underway. </li> <li>Cesar Rodriguez-Saona’s group at Rutgers has been applying chemical ecology techniques to understand the defensive traits of plants to the false blossom disease. Last year they evaluated the molecular and biochemical changes associated with plant defensive traits in cranberries affected by the false blossom disease and the preference and performance of its insect vector (blunt-nosed leafhoppers) and leaf chewers (spotted fireworm, Sparganothis fruitworm, and gypsy moth) on plants infected by false blossom disease.</li> <li>This same groups has been very active at development management tools based in behavior-manipulation to control the invasive pest spotted wing drosophila (SWD) in blueberries. These studies involved the use of attracticidal red spheres that incorporate a toxin, a phagostimulant, and a visual stimulus. Experiments were conducted to evaluate: a) the effects of pattern of placement of spheres within fields (grid versus border) in reducing SWD infestation, and b) the effects of location of spheres within a bush (top versus bottom) in reducing SWD infestation. Studies were also conducted using a new sprayable attract-and-kill formulation, SPLAT SWD, to reduce SWD infestation. SPLAT SWD was applied alone or in combination with organic insecticides in blueberry fields. In addition studies were conducted to investigate the response of SWD to odors from various sources including fermentation, yeast, and leaves. These studies were conducted under laboratory and field conditions.</li> <li>The group of Andre Kessler studied how biotic and abiotic environmental factors influence chemical information transfer and plant secondary metabolism-mediated interactions with other organisms. This past year, they focused on three key projects, namely A) the effects of temperature and humidity on the information : noise ratio in volatile organic compound (VOC) signaling, B) the effects of certain soil elements, such as As and Si on constitutive and inducible plant secondary metabolism and herbivore resistance, and c) the role of VOC signaling on mediating complex community dynamics and plant fitness outcomes. One major finding from the Datura wrightii study system is that the emission of certain plant VOCs is primarily altered by abiotic stresses, while others are emitted specifically in response to biotic stresses, such as herbivory. This means that VOC-mediated chemical information is encoded in distinct channels allowing interacting organisms to very specifically extract information about the plant’s physiological and metabolic status. In another study with cucumber, the group found a major induced resistance-mediating effect of Si. Plants grown in soils with minimal Si-content were not able to induce resistance in response to herbivore attack. Current work focuses on the effects of Si on direct and indirect resistance traits as well as the mechanisms underlying the priming effect. Lastly, research associated with this Multistate project that focused on modeling chemical information transfer revealed VOC-mediated chemical information transfer has a stabilizing effect on community dynamics.</li> </ul>   Milestones reached: As a group we have reached several milestones pertaining to our different objectives. Most activities have been focusing on defining the variability of chemical mediated interactions between pests, crops and beneficial organisms in terms of plants chemistry, species interaction and landscape factors in the Northeast (Objective 2). Here we have an overall better understanding of which chemical cues are mediating interaction between cucumbers and their herbivores, how the landscape is shaping interaction between crops, herbivore pests, and predators, how plant quality can affect pollinator health and how the quality of the crop influence their interactions with herbivores. Regarding our second objective on developing chemical ecology tools and information to support sustainable agriculture by reducing damage by pests in crops such as potatoes, brassicas, cucurbits, apples, blueberries, and sweet corn, while maintaining pollinator health in agricultural systems we have definitively started to identify the main chemical cues that are involved in important interaction between plants and their pests or vectors of important diseases. Mostly for blueberry there are promising tools that can help control Spotted wing Drosophila, while other information could be used to hopefully be soon used as tools for more sustainable agriculture. Our 5th objective of establishing a chemical ecology analytical facility in the Northeast definitively is on their way and expertise among members of this multistate have allowed for shared technical expertise and equipment.

Publications

Glaum P. and A. Kessler. 2017. Functional reduction in pollination services through Herbivore-Induced Pollinator Limitation and its potential in mutualist communities. Nature Communications. in press Claflin, S, Jones, L, Thaler, J, Power, A. 2016. Crop-dominated landscapes have higher vector-borne plant virus prevalence. Journal of Applied Ecology. 10.1111/1365-2664.12831

Impact Statements

Grant applications: Mike Mazourek (Cornell University) and Brian Leckie (Tennessee Tech University): "Genetic Basis of Cucurbit Specialist Preference in Plants with Differing Domestication Biogeographies” to USDA NIFA-AFRI program. Lauren Brzozowski (Mazourek program) to Schmittau-Novak small grants program within Cornell's School of Integrated Plant Sciences. for $4976.20 to fund collaboration with graduate student in entomology to look at dual-RNAseq transcriptomics of insects and plants in our squash-striped cucumber beetle system. Pending USDA-NIFA-2017-06553. “How much, how far and why: Understanding variation and mechanisms for the medicinal effects of sunflower pollen.” L. S. Adler (PD), R. E. Irwin (co-PD), Q. S. McFrederick (co-PD), L. Rieseberg (co-PD), P. C. Stevenson (co-PD). 3/1/18-2/28/21. $999,996. 2017-20 USDA-NIFA-2016-07962. “Sunflowers as treatment and preventative for bumble and honey bee pathogens.” L. S. Adler (PD), R. E. Irwin (co-PD), Q. S. McFrederick (co-PD), J. D. Evans (co-PD), K. Bayliss, (co-PD), D. A. Delaney (Key Personnel). 4/15/17-4/14/20. $999,960.

Date of Annual Report: 03/10/2018

Report Information

Annual Meeting Dates: 01/11/2018 - 01/12/2018
Period the Report Covers: 11/19/2016 - 01/12/2018

Participants

Andre Kessler, Cornell University
Michael Mazourek, Cornell University
Susan Whitehead, Virginia Tech
Kyle Wickings, Cornell University
Katja Poveda, Cornell University
Cesar Rodriguez-Saona, Rutgers University
Shadi Atallah, University of New Hampshire
Jared Ali, Pennsylvania State University
Georg Jander, Boyce Thompson Institute

Brief Summary of Minutes

The group met on January 12, 2018 on the Cornell campus in Ithaca, NY. We had 9 participants attending the meeting that was led and organized by Katja Poveda and Andre Kessler. All participants, except for one (Georg Jander) had attended the previous meeting and about half the participants have currently funding while the other half don’t have funding through this multi-state initiative, but are interested in being part of the group and writing proposals together. This meeting was dedicated to obtain updates on the projects that people were involved, discuss the results and what they mean for sustainable management practices in the Northeast and to look for funding opportunities based on the preliminary data obtained.

The executive decisions that were made during this meeting, where:

that the next organizational meeting was going to be organized in Penn State University, PA and will be taking place in October or November 2018.

that the chair of the Executive Committee for the next year was going to be Jared Ali, the representative at large Gary Felton and that John Tooker would fulfill the role of secretary.

MEETING MINUTES (summary of main results and points discussed)

January 11, 2018

6 pm: arrival and dinner

January 12, 2018

9 am: Welcome remarks by Katja Poveda and Andre Kessler

9:15: Susan Whitehead

Susan presented her work on the evolutionary ecology of plant interactions as the focus in her lab. She noted that her current emphasis is on investigating fruit chemistry and their relations with seed predators, pathogens and dispersers. Her main areas of research are 1)the chemical ecology of seed dispersal and fruit defense, 2)plant evolutionary responses to multispecies interactions, and 3) causes and consequences of phytochemical diversity for plant interactions and 4) the consequences of domestication on defenses and interactions. Currenly her study systems are: a) Piper-bat interactions, b) apple domestication and resistance and c) Physalis interactions with herbivores and pollinators. Most of the time was spend discussing two of her current research proposals that were:

Managing the apple phytobiome for enhanced fruit protection, nutrition and yield

Sensory systems of fruits bats as a model for improving robotics in precision agriculture

The rest of the time was spend giving Susan feedback on the proposed projects and the granting agencies she could apply for.

9:50: Andre Kessler:

Andre gave an overview of his study systems, which include tobacco, goldenrod, tomato, maize (push-pull). Specifically funded by the multistate he has been working on the VOC-mediated information transfer and pest control. His lab has been working on how to manipulate information transfer between plants and their insect pests and how this can be applied in the field, where the information could be manipulated. He also presented work on the importance of SI (Silicon) on the inducibility of the secondary metabolisms in cucumber.

10:21: Jared Ali

Jared started presenting on the technology available in Penn State for volatile collection above and belowground. This was in order to promote collaboration with his lab and ensure that all members of this multistate group have a clear understanding of the equipment available and the type of analysis that can be performed in his lab.

He also presented on his research on how entomopathogenic nematode infestation can reduce the mass and oviposition of CPB feeding on a plant, which talks for the indirect effect of EPN mediated by VOC’s and not just the direct effect. In addition he presented research on how the odors of predators (Stinkbugs and ladybeetles) can prime the plants and affect plant-herbivore interactions. The application would be to induce plants both belowground and aboveground to affect herbivory. He also presented fascinating data on how the chitinases in the frass are affecting the induction of plants and how touching plants can also affect volatiles. He hereby showed that plants can be elicitated by non-conventional means, such as proteins in the frass (and not in the saliva), responses to “touch” and also responses to neighboring plants that have been “touched”.

His newest project presented shows how cover crops can affect Arbuscular Mycorrhizal Fungi (AMF) Communities and how the careful selection of those cover crops will allow to choose cover crops that facilitate the establishment of AMF while avoiding the use of those cover crops that inhibit the growth of those AMF.

11:00 Shadi Atallah

Shadi presented on his new multistate project that was born through the previous multistate meeting on “Bioeconomics of agrobiodiversity, pest control and pollinator health”. Shadi brings a completely different perspective to our meetings, since he is an economist, broadening our understanding of the implications that our research might have in terms of their economic impact. In their work they have been looking at the trade-offs between productivity, enabled through the extensive use of external inputs and pollination services. The main objective of the project is to determine if the use of neonicotinids as seed coating, while permitting the effective control of pests, could have a hidden costs due to their negative effects on pollinator health. This work that has also been expanded to an SCRI project led by Ian Kaplan, another member of this multistate group, where this tradeoffs between plant protection and pollination are observed throughout multiple states in different cucurbit plants. More recently in a project led by Katja Poveda, an in collaboration with Scott Mc Art, Brian Nault, Zsofia Szendrei and Ian Kaplan, we have expanded this idea to also include squashes that are so important in the North East. Shadi is currently building models to look at the effects of neonicotinoids depending on the spray, the run-off and the also natural habitats than can protect them from the insecticide use.

Shadi, through a proposal funded by this multistate, is also looking at the importance of variety biodiversity on the insurance value of agrobiodiversity in apple orchards. This project includes a model in which they design an optimal orchard spatial design that will minimize pest damage and the use of insecticides. The main idea is that by taking into account variety resistance and tolerance an optimal orchard can be designed that through its configuration will minimize damage and maximize productivity.

11:30 am: Kyle Wickings

Kyle talked about his program on the chemical ecology in the rhizosphere. His research focuses on how fungi collected from turf affect root herbivory by grubs. His results show that some fungi inoculations cause more feeding, but that Beauviera (entomopathogenic fungi) caused a reduction in root tissue removal by grubs compared to control plants. The roots of those plants have a higher carbon:nitrogen ratio.

He also presented on his work on how herbivores can change the soil composition and how this understanding could help manage the use of neonicotinoids in turf. He hypothesizes that root herbivores are affecting the SOM content in the environment through their faeces and also through the root leftover that they leave after feeding on the plants. This extra SOM in the soil should increase the emission of CO2 and be attractive to ovipositing females, which should prefer those high SOM spots for oviposition and better larval development. Given that those hot-spots of grubs actually exists, if they can be identified through the emission of CO2 in the soil, it would be possible to detect future hotspots and just treat those spots with neonicotinoid, reducing more effectively and in a targeted manner pest pressure in turf. We discussed potential funding sources for this ideas and identified sources such as NSF: natural-human impacts: NSF CHN (Couples human-natural systems) as non-conventional sources that could be interested in funding this.

LUNCH:

This year for the first time we invited students, postdocs and visiting professors to our lunch to lead a discussion of the impact of context dependency on chemical-ecology tools for agriculture. Questions that were discussed were:

-How do we deal with context dependency of chemical ecology processes from the individual to the landscape scale? We realized that in the context of precision agriculture, it is very important to address the concept of context dependency, to be able to provide effective tools that can be implemented in different context. At the end of the lunch we concluded that the best approach to test this would be to set up a project across the US where we test the same approach (for example volatile induced responses, push-pull systems, pheromone traps, etc) across different sites in the US and monitor its context dependency. We would repeat an experiment across multiple crops and multiple states. We would need to agree on one method and experiment that data can be compared across.

We thought that it would be ideal to pitch the idea to the McKnight foundation and explore other venues of funding such as the USDA-NIFA SCRI. Students and postdoc where very excited of being part of this discussion and overall this was seen as a positive outcome for everybody.

2:20 pm: Cesar Rodriguez-Saona

Cesar presented his research on how domestication can affect plant defenses against herbivores. His questions include: 1) Are there trade-offs between selection for high plant yield and defense? And 2) How does pathogen infection affect multi-tropic level interactions? He presented a case study on blueberry domestication and the preference and performance for Drosophila suzukii.

He also presented some more applied work on the use of semiochemicals (attractants, repellents, volatiles, pheromones) to manipulate insect behavior and reduce pest populations. For example they look at the effect of the phytoplasma (False Blossom Infection) on herbivores (vectors and non-vectors). In general the phytoplasma increases the preference for the herbivores, although the plants are doing really bad.From his experience he says that commercializing a “chemical ecology”solutions is really complicated and can be a complication for really making a difference

2:50 pm: Katja Poveda

Katja presented her work on overcompensation and more specifically how the damage in one generation can lead to an overcompensatory response in the next generation. There was a lot of interest in this, since it could be a solution for organic farmers who wan to improve tuber seed quality and yields. There was a discussion that this would be an ideal project to submit for an USDA-OREI, proposing it as a solution for organic agriculture to increase productivity.

3:30 pm: Mike Mazourek

Mike presented on how work on the domestication of squash and zucchini in organic farms and how to control pests in a sustainable way. The main pest he is trying to control is the striped cucumber beetles. He has been exploring how two varieties that are really different in their vulnerability for beetles, differ in their secondary metabolites. He has also been involved in outreach where he has been giving tasting and sustainability talks, that are very attractive to the public and he proposes this as a great way to reach a broader group of people and also to get more attention to how sustainability issued impact the food we eat.

Accomplishments

Outputs: The most significant outputs has been the writing of research proposal based on preliminary data gathered since the establishment of this multistate project. For example for the project focused on the control of herbivores of cucurbits, two new projects have been submitted (see below) and one has already been approved for funding. New funded projects that originated from this multistate include projects concerned with the conservation of monarch butterflies, through a better understanding of the interactions with milkweeds and also Also projects investigating the trade-offs between crop protection and pollination services have been initiated that involve PI’s with expertise in pollination, abricultural economics, crop protection, landscape ecology and groecology. Manuscripts have been submitted and published during this time (for details see impact statement below). Most PI’s involved in this multistate have also disseminated their results at national conferences like the Ecological Society of America meeting and the Entomological Society of America meeting. PI’s have also interacted with farmers, and other stakeholders such a beekeepers and crop breeders, to start establishing means by which the performed research can be translated to tools and management strategies to protect pollinators, reduce pest pressure and increase yields. Outreach events that includes tastings of new varieties coupled with sustainability talks have also allowed to reach the general NYS public. Our collaboration with the Northeast IPM center has also rendered us a piece in their newsletter (<a href="http://www.northeastipm.org/about-us/publications/ipm-insights/plants-have-natural-defense-systems/">http://www.northeastipm.org/about-us/publications/ipm-insights/plants-have-natural-defense-systems/</a>) that describes the objectives of this multistate and allows us to disseminate the importance of tools based on chemical ecology for more sustainable crop production.   Activities: <ul> <li>Related with our first and second objective, the project focused on controlling herbivores of cucurbits (lead by Mike Mazourek, Cornell University) has developed assays for the highly sensitive quantification of cucurbitacins using SPE concentration and LC-MS. This technique is used for sampling squash seedlings that define different taxonomic groups including inter and intraspecific comparisons that differ in their degree of damage by striped cucumber beetles. No differences were found for true leaves although they are most conspicuously damaged plant tissue in the field and further they were below the detection thresholds of the herbivore. Cotelydon differences aligned with beetle preference and were within beetle detection thresholds. This group hypothesized that beetle preference in squash is not determined by cucurbitacin concentration. To test this hypothesis, they exposed young seedlings of highly preferred squash (golden zucchini) and compared damage to non-preferred squash seedlings (summer squash). Comparisons were performed with either cotyledon or true leaves removed. In each experiment the beetles preferred golden zucchini tissue over the corresponding tissue in summer squash. The group interpreted this to mean that beetle feeding preferences are determined by another factor, other than cucurbitacins. This group has also adapted high resolution carotenoid separation methods to our HPLC system and calibrated it with known standards. Experiments are underway to look at carotenoid accumulation in different plant tissues that also exhibit preference differences by striped cucumber beetles.</li> <li>Regarding our second objective (Define variability of chemically mediated interactions between pests, crops, and beneficial organisms in terms of plant chemistry, species interactions and landscape factors in the Northeast), one group lead by Jennifer Thaler and Katja Poveda started a project measuring the relationship between potato plants, Colorado potato beetles and their predators on organic farms in Central New York. These farms were chosen to reflect a gradient from low-levels of agriculture to high levels of agriculture in the surrounding landscape. Preliminary data indicate that herbivore responses to predators depend on the landscape complexity. Jennifer Thaler’s group also investigated the defensive responses of Colorado potato beetles to stink bug predators using a population of beetles from Ithaca, NY. They have found large decreases in feeding and growth of beetles when predators are present but not consuming beetles. Combining these results is an advance in understanding the causes of variation in the predator-prey interaction and will be helpful in designing biological control practices in the future.</li> <li>In the front of pollinator research Lynn Adler has been leading an effort to understand how pollinator populations can be supported based on the quality of the host plants. This past year, they discovered that the medicinal value of sunflower pollen extends to a wide range of sunflower cultivars, wild sunflower accessions, two other Helianthus congeners, and even two Solidago species, which are in the same family as sunflower but not very close relatives. This discovery suggests that a wide range of sunflower relatives may be beneficial to the common eastern bumble bee and useful for treating Crithidia infection.</li> <li>The group lead by Richard Karban in this past year has learned how to make more effective use of volatile communication to induce resistance against insect herbivores. Specifically, they have learned that variation in the nutritional quality of crops can reduce the efficiency and success of herbivores across many different species of plants and insects. They also identified important sources of variation in plant quality in their model system for plant communication, Artemisia tridentata. Individuals vary in the major chemicals that they emit when they are attacked or damaged. This chemotypic variation affects how effectively they respond to cues of damage. The effectiveness of communication also is affected by the geographic proximity of the source of volatile cue, suggesting that plant cues may exhibit geographic dialects.</li> <li>Anurag Agrawal’s groups has been investigating ways to aid to the conservation of non-target organisms such as the monarch butterfly to agricultural practices, specifically the use of herbicides. Specifically they are investigating the use of swallow-worts by monarch butterflies, which are used for oviposition but do not support caterpillars. In this project they are investigating the use of swallow-worts by monarchs, the chemical cues used by monarchs to recognize them, and the impacts of reduced milkweed availability due to herbicide usage on their preferences. Initial experiments showed reduced oviposition on swallow-wort in the presence of milkweed. Chemical analyses are currently underway. </li> <li>Cesar Rodriguez-Saona’s group at Rutgers has been applying chemical ecology techniques to understand the defensive traits of plants to the false blossom disease. Last year they evaluated the molecular and biochemical changes associated with plant defensive traits in cranberries affected by the false blossom disease and the preference and performance of its insect vector (blunt-nosed leafhoppers) and leaf chewers (spotted fireworm, Sparganothis fruitworm, and gypsy moth) on plants infected by false blossom disease.</li> <li>This same groups has been very active at development management tools based in behavior-manipulation to control the invasive pest spotted wing drosophila (SWD) in blueberries. These studies involved the use of attracticidal red spheres that incorporate a toxin, a phagostimulant, and a visual stimulus. Experiments were conducted to evaluate: a) the effects of pattern of placement of spheres within fields (grid versus border) in reducing SWD infestation, and b) the effects of location of spheres within a bush (top versus bottom) in reducing SWD infestation. Studies were also conducted using a new sprayable attract-and-kill formulation, SPLAT SWD, to reduce SWD infestation. SPLAT SWD was applied alone or in combination with organic insecticides in blueberry fields. In addition studies were conducted to investigate the response of SWD to odors from various sources including fermentation, yeast, and leaves. These studies were conducted under laboratory and field conditions.</li> <li>The group of Andre Kessler studied how biotic and abiotic environmental factors influence chemical information transfer and plant secondary metabolism-mediated interactions with other organisms. This past year, they focused on three key projects, namely A) the effects of temperature and humidity on the information : noise ratio in volatile organic compound (VOC) signaling, B) the effects of certain soil elements, such as As and Si on constitutive and inducible plant secondary metabolism and herbivore resistance, and c) the role of VOC signaling on mediating complex community dynamics and plant fitness outcomes. One major finding from the Datura wrightii study system is that the emission of certain plant VOCs is primarily altered by abiotic stresses, while others are emitted specifically in response to biotic stresses, such as herbivory. This means that VOC-mediated chemical information is encoded in distinct channels allowing interacting organisms to very specifically extract information about the plant’s physiological and metabolic status. In another study with cucumber, the group found a major induced resistance-mediating effect of Si. Plants grown in soils with minimal Si-content were not able to induce resistance in response to herbivore attack. Current work focuses on the effects of Si on direct and indirect resistance traits as well as the mechanisms underlying the priming effect. Lastly, research associated with this Multistate project that focused on modeling chemical information transfer revealed VOC-mediated chemical information transfer has a stabilizing effect on community dynamics.</li> </ul>   Milestones reached: As a group we have reached several milestones pertaining to our different objectives. Most activities have been focusing on defining the variability of chemical mediated interactions between pests, crops and beneficial organisms in terms of plants chemistry, species interaction and landscape factors in the Northeast (Objective 2). Here we have an overall better understanding of which chemical cues are mediating interaction between cucumbers and their herbivores, how the landscape is shaping interaction between crops, herbivore pests, and predators, how plant quality can affect pollinator health and how the quality of the crop influence their interactions with herbivores. Regarding our second objective on developing chemical ecology tools and information to support sustainable agriculture by reducing damage by pests in crops such as potatoes, brassicas, cucurbits, apples, blueberries, and sweet corn, while maintaining pollinator health in agricultural systems we have definitively started to identify the main chemical cues that are involved in important interaction between plants and their pests or vectors of important diseases. Mostly for blueberry there are promising tools that can help control Spotted wing Drosophila, while other information could be used to hopefully be soon used as tools for more sustainable agriculture. Our 5th objective of establishing a chemical ecology analytical facility in the Northeast definitively has progressed. Embedded in our presentations PIs overseeing chemical equipment have been talking about the current facilities making those equipments available for others and providing a good underatsnding of which type of analysis can be done in the different labs. The shared expertise among members of this multistate have allowed for the availability of shared equipment across the NE, fulfilling this objective.   Training Several postdocs, technician and PhD students have been trained on this project. They are not just receiving training on the chemical ecology of plant interactions and their potential use for sustainable agriculture, but also receiving substantial professional development.   Planned activities for the next year In the coming year, several groups (Mike Mazourek, Jennifer Thaler, Andre Kessler, Lynn Adler, Cesar Rodriguez, Anurag Agrawal) will finalize the analysis of their initial results and write those for publication. We anticipate that at least 7 manuscripts will be send out for publications derived from the data obtained this year. Also grant proposal will continue to be written based on preliminary data generated in the course of this multistate. We also anticipate that more concrete work with stakeholders such as organic farmers will allow us to submit a larger OREI proposal and that we will start implementing some of the gathered information in form of concrete tools or management practices on farms to support more sustainable agriculture (Objective 1). We will continue developing all proposed objectives, given that new funding was given to groups that are interested in characterizing the non-target effects of pesticides on pollinators, covering our goals proposed in objective 3. All groups that have obtained funding through this multistate will also present the results to the research community at national meetings and will disseminate their work also at local farmer meetings.

Publications

Vannette RL and Fukami T, Contrasting effects of yeast and bacteria on floral nectar traits, Annals of Botany, accepted. Rering C.C, Beck J.J., Hall, G., McCarthy, M., Vannette RL, Nectar-inhabiting microorganisms influence nectar volatile composition and attractiveness to a generalist pollinator. New Phytologist (early view) doi: 10.1111/nph.14809. Glaum P. and A. Kessler. 2017. Functional reduction in pollination services through Herbivore-Induced Pollinator Limitation and its potential in mutualist communities. Nature Communications. in press Claflin, S, Jones, L, Thaler, J, Power, A. 2016. Crop-dominated landscapes have higher vector-borne plant virus prevalence. Journal of Applied Ecology. 10.1111/1365-2664.12831   Lauren Brzozowski and Michael Maozurek. Sustaining the future of horticultural crop production through organic agroecological pest management. Sustainability. Accepted. Brevik, K., S. D. Schoville, D. Mota-Sanchez, and Y. H. Chen. 2018. Pesticide durability and the evolution of resistance: A novel application of survival analysis. Pest Management Science 10.1002/ps.4899. Schoville, Sean D., Y. H. Chen, M. N. Andersson, J. B. Benoit, A. Bhandari, J. H. Bowsher, K. Brevik, K. Cappelle, M-J. M. Chen, A. K. Childers, C. Childers, O. Christiaens, J. Clements, E. N. Elpidina, P. Engsontia, M. Friedrich, I. García-Robles, C. Goswami, A. Grapputo, K. Gruden, M. Grynberg, B. Henrissat, E. C. Jennings, J. W. Jones, M. Kalsi, S. A. Khan, A. Kumar, F. Li, V. Lombard, X. Ma, A. Martynov, N. J. Miller, R. F. Mitchell, M. Munoz-Torres, A. Muszewska, Brenda Oppert, S. R. Palli, K. A. Panfilio, Y. Pauchet, L. C. Perkin, M. Petek, M. F. Poelchau, E. Record, J. P. Rinehart, H. M. Robertson, A. J. Rosendale, V. M. Ruiz-Arroyo, G. Smagghe, Z. Szendrei, E. M. Szuter, G. W. C. Thomas, A. S. Torson, I. M. Vargas Jentzsch, M. T. Weirauch, A. D. Yates, G. D. Yocum, J-S Yoon, Stephen Richards. 2018. A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Scientific Reports 8: 1931. Brevik, K., L. Lindström, S. D. McKay, and Y. H. Chen. 2018. Transgenerational effects of insecticides – implications for rapid pest evolution in agroecosystems. Current Opinion in Insect Science. Special Issue, “Ecological Adaptation in Agroecosystems”. Izzo, V., Y. H. Chen, S. D. Schoville, C. Wang, D. J. Hawthorne. 2018. Origin of pest lineages of the Colorado potato beetle, Leptinotarsa decemlineata. Journal of Economic Entomology. Crossley, M. S., Y. H. Chen, R. L. Groves, and S. D. Schoville. 2017. Landscape genomics of Colorado potato beetle provides evidence of polygenic adaptation to insecticides. Molecular Ecology DOI: <a href="http://10.1111/mec.14339">10.1111/mec.14339</a> Alyokhin, A. and Y. H. Chen. 2017. Adaptation to toxic hosts as a factor in the evolution of insecticide resistance. Current Opinion in Insect Science 21:33-38.

Impact Statements

Grants applied for: 1. Improved antagonists for control of fireblight in apple and pear. Source: USDA-Specialty Crop Multistate Program Amount: $554,676 Duration: July 1, 2018-June 30, 2020 Role: PI Location of project: Davis, CA; Pullman, WA, Gainesville, FL Person-months of year: 1 2. Screening potential antagonists for fire blight control Source: CA Pear Board Amount: $9,972 Start Date/Duration: July 1, 2018-June 30, 2019 Role: PI Location of Project: Davis, CA Person-months per year: 0.5 3. Dimensions: Collaborative research: Microbial mediators of pollination: Linking phylogenetic, genomic and functional diversity of microbial communities in nectar Source: National Science Foundation Amount: $1094730.00 Duration: 5 years Start Date/Duration: Jan 1, 2019-Dec 31, 2023 Mike Mazourek (Cornell University) and Brian Leckie (Tennessee Tech University): "Genetic Basis of Cucurbit Specialist Preference in Plants with Differing Domestication Biogeographies” to USDA NIFA-AFRI program. Lauren Brzozowski (Mazourek program) to Schmittau-Novak small grants program within Cornell's School of Integrated Plant Sciences. for $4976.20 to fund collaboration with graduate student in entomology to look at dual-RNAseq transcriptomics of insects and plants in our squash-striped cucumber beetle system. USDA-NIFA-2017-06553. “How much, how far and why: Understanding variation and mechanisms for the medicinal effects of sunflower pollen.” L. S. Adler (PD), R. E. Irwin (co-PD), Q. S. McFrederick (co-PD), L. Rieseberg (co-PD), P. C. Stevenson (co-PD). 3/1/18-2/28/21. $999,996. 2017-20 USDA-NIFA-2016-07962. “Sunflowers as treatment and preventative for bumble and honey bee pathogens.” L. S. Adler (PD), R. E. Irwin (co-PD), Q. S. McFrederick (co-PD), J. D. Evans (co-PD), K. Bayliss, (co-PD), D. A. Delaney (Key Personnel). 4/15/17-4/14/20. $999,960.

Date of Annual Report: 02/05/2019

Report Information

Annual Meeting Dates: 11/01/2018 - 11/02/2018
Period the Report Covers: 01/01/2018 - 01/01/2019

Participants

Jan Nyrop, Cornell
Jared Ali, Penn State
John Tooker, Penn State
Gary Felton, Penn State
Anurag Agrawal, Cornell
Jennifer Thaler, Cornell
Ivan Hiltpold, Univ. Delaware
Denis Willet, Cornell
Rick Karban, UC Davis
Cesar Rodriguez-Soana, Rutgers
Mary Purcell, USDA-NIFA
Tom Baker, Penn State
Jim Tumlinson, Penn State
Tanya Renner, Penn State
Kelli Hoover, Penn State
Etya Amsalem, Penn State

Brief Summary of Minutes

The group met on November 1-2, 2018 on the Pennsylvania State University campus in University Park, PA. We had 16 participants attending the meeting that was led and organized by Jared Ali. We had many first time participants, including special virtual participation from USDA-NIFA Program manager, Dr. Mary Purcell. Our goal was to discuss new results and what they mean for sustainable management practices in the Northeast and to look for funding opportunities based on the preliminary data obtained. To this end, we had a specific theme for this meeting: “Turning our biological discoveries into useful applications”. The day was structured into two sessions The first session comprised of talks by each PI geared to touch on the following three topics: A) Talk about how your research has made an applied contribution with specific discussion of what the key features lead to this success, B) Discuss a result you have that you think could be applied, point out what you think the stumbling blocks to application are and get feedback on making this jump, and C) Discuss a totally fundamental idea that you think people with an applied focus should be taking into consideration. In the second session we had a larger group discussion on how we could begin a Chemical Ecology Network of research along the lines of a coordinated research program.

The executive decisions that were made during this meeting were:

That the next organizational meeting was going to be organized again at Penn State University, PA (unless after polling the members not present via email we have an alternative suggestion) and it will be taking place in October 2019.

That the chair of the Executive Committee for the next year was going to be Jared Ali, the representative at large Gary Felton and that John Tooker would fulfill the role of secretary.

We decided to initiate a coordinated project with Phyto hormones (JA/SA) and will be lead by Drs. Rodriguez-Soana and Whitehead.

MEETING MINUTES (summary of main results and points discussed)

General Topic of this year’s meeting and talk format: “Turning our biological discoveries into useful applications”

1) Morning ession

Talks per PI in one or all three flavors(1,2, or 3). These 3 flavors should cover the range of interests in the group.

Talk about how your research has made an applied contribution with specific discussion of what the key features lead to this success

Talk about a result you have that you think could be applied, point out what you think the stumbling blocks to application are and get feedback on making this jump

Have a totally basic idea that you think people with an applied focus should be taking into consideration

2) Afternoon Discussions

Breakout groups led by John, Ivan, or Jennifer. People at the meeting may come up with more ideas or these could come from the research presentations.

3) Writing a Paper for JOCE/ ideas? Can we Make a ChemECO Network program (JA/SA) via USDA or NSF Research Coordination Network (RCN) program

Agenda

Thursday: 6 pm group dinner

Friday meeting in 118 Ag Science Building (ASI)

8:30 Breakfast

9:00 Welcome

9:05-10:05: 7 talks (4-minute talk, 4-minute discussion) (Cesar, Jennifer, Denis, Ivan, Rick, Gary, John)

10.05-10:15: break

10:15-11:15: 6 talks (4-minute talk, 4-minute discussion) (Tanya, Etya, Jared, Anurag, Kelli, Jan, Tom)

11:15-12:00: Mary Purcell- NIFA opportunities

12:00- 12:05: Group photo

12:05-1:30: Lunch (Student and Postdocs included)

1:30-2:00: Organizational meeting (Annual report, choosing next leadership, next meeting time and location)

2:00-2:45: Topical Research Brainstorming

2:45-3:30: Reconvene

3:30-4:15: Topical Research Brainstorming

4:15-5:00: Reconvene and goals (Research Coordination Network)

Accomplishments

Activities/Milestones: <ul> <li>This year, Richard Karban’s group focused on two aspects of host plant resistance – understanding volatile cues that trigger induced resistance and understanding the role of plant surfaces as a means of defense against herbivores) Previously, they found that the volatile cues emitted by experimentally clipped sagebrush plants could be categorized into two chemotypes. During the past season, they characterized additional chemotypes and continued to examine the specificity of cues from these chemotypes at inducing resistance against chewing herbivores. Their goal is to determine the specificity of communication between plant individuals and to identify biologically active components of the volatile blends. ii.) They continued investigations of sticky plants. These plants often catch sand, which provides a physical barrier that deters herbivores. The sand interferes with consumption and digestion. Sticky plants also catch small insects, which attract specialized predatory bugs that protect the plants against herbivores.  We also continued work examining the unidirectional hairs of many grasses. These hairs usher small insects to leaf tips and away from valuable grass meristems.</li> </ul> <ul> <li>Over the past year the group lead by Scott McArt accomplished several of their multi-state chemical ecology project goals. They successfully conducted the main field experiment on 22 farms, supplementing with bumble bees on 11 of the 22 farms. They obtained data on landscape composition around the farms, pest populations, bee abundance and diversity, and spray practices. They are currently screening 330 bees (15 per farm) for pesticide residues (291 potential compounds) and pathogens (via a 5-pathogen multiplex). An undergraduate student (Casey Hale) is conducting the screens on the 330-bee dataset for her Honors thesis. In addition, they submitted our first manuscript for publication from this work (to Apidologie) — the manuscript is currently in review. </li> </ul> <ul> <li>The Adler lab has made significant progress in pollinator health. They have published our original findings that sunflower pollen reduced Crithidia in B. impatiens, reduced Nosema in Apis mellifera, and that more sunflower acreage was associated with lower Crithidia infection in wild-caught B. impatiens (Giacomini et al 2018). They’ve prepared two manuscripts for publication, one of which is now submitted and one which is close to submission. The submitted manuscript demonstrates that pollen from many cultivated sunflower cultivars, wild populations, two congeners, and Solidago, a distant relative in the same family, all reduce Crithidia in B. impatiens relative to buckwheat pollen, and most relative to sunflower pollen (LoCascio et al in review). The other manuscript, which should be submitted in the next month, asks how timing of exposure to sunflower pollen during foraging or after infection affects Crithidia infection in B. impatiens. They’ve found that exposure to sunflower pollen during foraging does not influence infection, but the timing and duration of sunflower pollen after inoculation both affect infection outcomes. Their research is allowing them to identify whether and under what conditions sunflower supplements could be developed and marketed for commercial bumble or honey bee rearing. So far, results seem more promising with bumble than honey bees.</li> </ul> <ul> <li>Yolanda Chen and her research group has meet a major accomplishment this past year. They were able to publish the genome paper on the Colorado potato beetle (CPB) (Schoville et al. 2018). They studied the beetle genome for evidence of genomic features that could contribute to the beetle’s ability to evolve rapidly. Transposable elements contribute to least 17% of the beetle’s highly fragmented genome, suggesting that they may be a larger portion of a completed genomes. We found that the beetle has expansions in gene expansions in digestive enzymes and gustatory receptors. However, contrary to our expectations, CPB does not show expansions in gene families associated with detoxification. We have also found that CPB ranks as one of the fastest to evolve resistance to insecticides (Brevik et al. 2018). We also published a phylogeographic history study on CPB showing that the pest populations are derived from plains beetles, and beetles in the southwestern US are more similar to Mexico. Finally, we also published a conceptual paper on transgenerational effects of insecticides (Brevik et al. 2018), as part of a special issue in Current Opinion in Insect Science titled, “Ecological Adaptation in Agroecosystems”.</li> </ul> <ul> <li>Kelli Hoover’s group completed studies on impact of phenolic glycosides on Asian longhorned beetle; began studies on pollinator deficiency of black cherry in Pennsylvania; began studies on plant-insect interactions and the requirement for tree-of-heaven for development of spotted lanternfly (SLF) on woody ornamentals and in forest systems. They determined that there is resource partitioning by Asian longhorned beetle and adults on poplars in response to high levels of phenolic glycosides in bark (fed on by adults), but not wood (fed on by larvae). The group also demonstrated that the fungal gut symbiont of ALB is transmitted from mother to offspring during oviposition. In addition, they documented that lepidopterans feeding on the same host plant in the same part of the plant and the same field harbor different gut microbial communities, likely due to an environment X genetic interaction. Lastly, they figured out how to rear spotted lanternfly under greenhouse conditions in quarantine; also set up field experiment with planted trees in replicated plots in SLF quarantine zone to investigate differences in SLF performance on different host plants.</li> </ul> <ul> <li>Work in Susan Whitehead’s lab is relevant to two of the major goals of the multistate project: (1) Develop chemical ecology tools and information to support sustainable agriculture by reducing damage by pests in crops such as potatoes, brassicas, cucurbits, apples, blueberries, and sweet corn, while maintaining pollinator health in agricultural systems, and (2) Assess the impact of domestication on plant and animal chemical ecology in agricultural fields and identify unifying patterns of human and natural selection on chemical interactions of crop plants.We focus on apples as a model system to address these goals. Apples produce a diversity of both volatile and non-volatile secondary metabolites that could function in defense, but their effects on herbivores and natural enemies are almost entirely unexplored. Furthermore, nothing is known about how apple chemical defenses may have been altered during domestication. Our research this year focused on chemical analyses and integrating and analyzing data from past experiments to examine: 1) how apple fruit chemistry mediates resistance to fruit-feeding insects, 2) how fruit chemistry changes in response to insect feeding, and 3) how fruit chemistry has changed during apple domestication. Given that insecticides cost US farmers over $4.3 billion annually, understanding and harnessing natural fruit defenses could be a promising tool to increase the economic and environmental sustainability of apple production.</li> </ul> <ul> <li>In this reporting period, Rachel Vannette’s group worked to quantify microbial effects on floral nectar traits and their effects on pollinators, including bumble bees. They worked with the commercially available B. impatiens and assessed their preference for solutions modified by different microbial inhabitants. The results, which are currently being written up for publication, indicate that Bombus workers exhibit strong and consistent preference for specific microbial inhabitants of floral nectar, driven by both taste and scent. They are continuing to follow up on this work in both impatiensand the native B. vosnesenskii. In another project, they worked to identify variation among plant genotypes of the California native plant Epilobium canumin floral chemistry traits and relate this variation to patterns of pollinator visitation. They found that floral traits were indeed variable among plant cultivars and were linked to variation in pollinator visitation, including by hummingbirds, honey bees and carpenter bees. Different plant traits were associated with visitation by each group of organisms. They also analyzed the effects of potential microbial antagonists in pear against the pathogen Erwinia amylovoraon nectar characteristics.</li> </ul> <ul> <li>Ivan Hiltpold and his research team have demonstrated in a field setting that birds respond to synthetic blends of herbivore induced plant volatiles typically emitted by corn damaged by fall armyworm (FAW) caterpillars. Significantly more attacks and pecks were observed on plasticine caterpillars close to HIPVs dispensers than on plasticine caterpillars in the vicinity of dispensers containing solvent only. In an oviposition trial, they’ve demonstrated that FAW female significantly avoid corn plants previously induced by conspecific larvae. Larvae raised on FAW induced plants developed significantly slower and less individuals metamorphosed into pupae. Finally, they are currently describing a new tritrophic interactions between slugs, soybean and ground beetles. Data is being collected in 6-arms olfactometers and HIPVs qualified and quantified.</li> </ul> <ul> <li>The Agrawal group has now completed two large scale experiments, one on several varieties of sweet potato and the other on lettuce.  In both cases, they conducted multi-factorial experiments on domestication, induced resistance to insects, and the role of plant produced latex in mediating these effects.  All data have been collected, although some chemical analyses of the plant tissues remain.  This winter they will be summarizing and compiling results for publication as well as to plan the next field season.  Initial results were presented at the Multi-State meeting at Penn State (Nov. 2018). They have been working with Michael Mazourek’s lab in Plant Breeding & Genetics at Cornell to continue this work and expand to cucurbits.</li> </ul> <ul> <li>This year, research lead by Jennifer Thaler addressed Objective 2 of the Multistate project. Little is known about population variation in predator- prey interactions even though it is critical for understanding how biological control agents will work in different locations. This year, we looked at variation in responses to predators between populations of Colorado potato beetles that are resistant or susceptible to insecticides. Colorado potato beetle is well- known for it’s ability to evolve resistance to insecticides, making it a difficult pest to control. In places with a history of intensive insecticide use, resistance has evolved. This may impact interactions with predators because resistant individuals have different behavior and physiology than susceptible individuals. This may impact the effectiveness of biological control agents in populations with resistant individuals.  This year, we studied three paired populations of insecticide resistant or susceptible Colorado potato beetles originating from four states (New York, Vermont/Maine, and Wisconsin). We collected 30 clutches beetle eggs from each of the six populations. In the lab at Cornell, they were transferred to fresh foliage to remove potential pesticide residues, and the eggs were hatched. The newly emerged beetle larvae from each population were divided into two treatments; larvae were either exposed to non-lethal predators or unexposed controls. The non-lethal predators were adult male Podisus maculiventris with the terminal segment of their beak removed to generate a predator that can hunt but not kill its prey. This allows us to measure the beetle responses to the presence of predators.  Last year, beetle larvae were exposed to the predator and control treatment for three days after which we measured their feeding and growth. This year, we extended these findings by measuring the fitness consequences of predator exposure in these populations. We did this by rearing beetles in the treatments through adult hood and measuring their egg production. We also collected beetles to assay their actual susceptibility to insecticide. We are currently analyzing this data.</li> </ul> <ul> <li>The group lead by Jared Ali has three recently funded projects. i)Cover crops legacy effects on plant resistance to herbivores: With recent funding from the USDA ($500,000 to PI Ali funded January 2018) they are investigating how multiple management components can be integrated to enhance plant resilience to stressors and improve productivity. We have found that the species of cover crop farmers choose has legacy effects on the subsequent corn crop’s resistance to the European corn borer, and that this legacy is mediated by soil fertility and/or mycorrhizal colonization. The goal of this proposal is to discover mechanisms that control the cascade of interactions linking cover crops, soil fertility, and corn pest management. ii) Using beneficial nematodes to prime plant resistance to pests: In this project we are studying chemical cues that play important roles in ecological interactions, especially among plants and invertebrates. A relatively recent and exciting discovery is that plants perceive and respond to chemical cues, often detecting herbivore-associated cues as a warning to prepare for future attack. Finding novel ways to harness these natural cues and organismal responses for enhancing crop protection represents a new frontier in agroecology. A major goal of this project is to elucidate indirect benefits of EPNs for plant protection against herbivores. iii)Monarchs, migrations and milkweed: We have initiated a pollinator health conservation project linking variation in milkweed defense biochemistry to variation in larval and resulting adult monarch butterfly fitness traits (NSF $897,841 funded May 2018). We are quantifying variation in plant toxicity traits within and across milkweed species using state-of-the-art methods in chemical ecology to determine how plant defense affects larval growth and subsequent adult fecundity, in reproductively active monarch butterfly cohorts. Using a combination of respirometry, flight kinematic analyses, and studies of lipid metabolism, we are examining how milkweed toxicity experienced during larval stages affects adult flight performance and energetics in migratory monarchs and will link these effects to expression of microRNAs controlling traits associated with migratory phenotypes. This project adds a novel perspective to typical chemical ecology practices to studying plant-herbivore interactions by examining physiological consequences of trophic interactions across the entire ontogeny of an herbivorous insect. The project substantially advances the knowledge of the basic biology of the iconic milkweed-monarch butterfly system, a model migratory insect with a complex ecology.</li> </ul> <ul> <li>Cesar Rodriguez-Saona lead a number of projects that align with the goals of the multi-state group. For project 1, They have conducted studies on the chemical ecology of the new invasive pest, spotted wing drosophila (SWD). They have evaluated two novel "attract-and-kill" strategies to control SWD: 1) attracticidal spheres; and 2) "SPLAT SWD Lure-and-Kill" (ISCA Technologies, Inc.). We conducted field studies in commercial blueberry farms to assess the protective capacity of attracticidal spheres and SPLAT SWD. With a second project they have conducted studies on the effects of phytoplasma infection on cranberry chemistry and its effects on the performance and preference of the vector, the blunt-nosed leafhopper. They’ve conducted no-choice and choice experiments. Phytoplasma-infected and non-infected cranberry plants were propagated and tested for differences in gene expression, phytohormones, and phenolic content.  A third project evaluates the effects of domestication on plant defenses against herbivores in blueberries. So far they have tested the preference of the new invasive pest, spotted wing drosophila, between wild and domesticated blueberries. Choice experiments were conducted and headspace volatiles were collected. These findings were presented at grower meetings and at scientific meetings. In 2018, this work was presented at the Entomological Society of America Annual Meeting (Vancouver, Canada), the Cumberland–Shenandoah Fruit Workers Conference (Winchester, Virginia), the International Society of Chemical Ecology Annual Meeting (Budapest, Hungary), and the Blueberry Open House (Hammonton, New Jersey).</li> </ul> Milesstones: As a group we have reached several milestones pertaining to our different objectives. Most activities have been focusing on defining the variability of chemical mediated interactions between pests, crops and beneficial organisms in terms of plants chemistry, species interaction and landscape factors in the Northeast (Objective 2). Here we have an overall better understanding of which chemical cues are mediating interaction between plants and their herbivores, how the landscape is shaping interaction between crops, herbivore pests, and predators, how plant quality can affect pollinator health and how the quality of the crop influence their interactions with herbivores. Regarding our second objective on developing chemical ecology tools and information to support sustainable agriculture by reducing damage by pests in crops such as potatoes, brassicas, cucurbits, apples, blueberries, and sweet corn, while maintaining pollinator health in agricultural systems we have definitively started to identify the main chemical cues that are involved in important interaction between plants and their pests or vectors of important diseases. For blueberry there are promising tools that can help control Spotted wing Drosophila, while other information could be used as tools for more sustainable agriculture. Our 5th objective of establishing a chemical ecology analytical facility in the Northeast has progressed. By further establishing ties between Cornell's and Pennstate's Chemical ecology Core groups and facilities we have begun to work out funding structures and pipelines to process samples and/or analyze behavior.  The shared expertise among members of this multistate have allowed for the availability of shared equipment across the NE, fulfilling this objective. Training  Several postdocs, technician and PhD students have been trained across these projects with planned travel and cooperation between universities. They are not just receiving training on the chemical ecology of plant interactions and their potential use for sustainable agriculture, but also receiving substantial professional development.  Planned activities for the next year In the coming year, we have planned to advance a chemical ecology research network of induced defenses across all of our agroecological systems. We anticipate that at least 10 manuscripts will be sent out for publications derived from the data obtained this year. Also grant proposals will continue to be written based on preliminary data generated in the course of this multistate.  We will continue developing all proposed objectives, given that new funding was given to groups that are interested in characterizing the non-target effects of pesticides on pollinators, covering our goals proposed in objective 3. All groups that have obtained funding through this multistate will also present the results to the research community at national meetings and will disseminate their work also at local farmer meetings.

Publications

<ol> <li>RJ Malik, JG Ali, JD Bever. Mycorrhizal composition influences plant anatomical defense and impacts herbivore growth and survival in a life-stage dependent manner. Pedobiologia 66, 29-35</li> </ol> <ol start="2"> <li>L Castano-Duque, A Helms, JG Ali, DS Luthe. Plant Bio-Wars: maize protein networks reveal tissue-specific defense strategies in response to a root herbivore. Journal of chemical ecology, 1-19</li> </ol> <ol start="3"> <li>D Markovic, I Colzi, C Taiti, S Ray, R Scalone, JG Ali, S Mancuso, Airborne signals synchronize the defenses of neighboring plants in response to touch. Journal of experimental botany 70 (2), 691-700 </li> </ol> <ol start="4"> <li>LoCascio GM, Aguirre L, Irwin RE and LS Adler (in review). Pollen from multiple sunflower cultivars and species reduces a common bumble bee gut pathogen. Proceedings of the Royal Society of London Series B.</li> </ol> <ol start="5"> <li>Giacomini JJLeslie J, Tarpy DR, Palmer-Young EC, Irwin RE and LS Adler. 2018. Medicinal value of sunflower pollen against bee pathogens. Scientific Reports 8: 14394. DOI: 10.1038/s41598-018-32681-y</li> </ol> <ol start="6"> <li>Chen, Y. H. and S. D. Schoville. 2018. Editorial Overview: Ecological adaptation in agroecosystems: Novel opportunities to integrate evolutionary biology and agricultural entomology. Overview for Special Issue titled, “Ecological Adaptation in Agroecosystems”. Current Opinion in Insect Science. 26: iv-viii. IF = 3.66, R = 12 out of 85 in Biology, R = 5 out of 93 in Entomology.</li> </ol> <ol start="7"> <li>Brevik, K., L. Lindström, S. D. McKay, and Y. H. Chen. 2018. Transgenerational effects of insecticides – implications for rapid pest evolution in agroecosystems. Special Issue, “Ecological Adaptation in Agroecosystems”. Current Opinion in Insect Science.https://doi.org/10.1016/j.cois.2017.12.007. IF = 3.66, R = 12 out of 85 in Biology, R = 5 out of 93 in Entomology.</li> </ol> <ol start="8"> <li>Brevik, K., S. D. Schoville, D. Mota-Sanchez, and Y. H. Chen. 2018. Pesticide durability and the evolution of resistance: A novel application of survival analysis. Pest Management Science 10.1002/ps.4899. IF = 3.25</li> </ol> <ol start="9"> <li>Schoville, Sean D., Y. H. Chen, M. N. Andersson, J. B. Benoit, A. Bhandari, J. H. Bowsher, K. Brevik, K. Cappelle, M-J. M. Chen, A. K. Childers, C. Childers, O. Christiaens, J. Clements, E. N. Elpidina, P. Engsontia, M. Friedrich, I. García-Robles, C. Goswami, A. Grapputo, K. Gruden, M. Grynberg, B. Henrissat, E. C. Jennings, J. W. Jones, M. Kalsi, S. A. Khan, A. Kumar, F. Li, V. Lombard, X. Ma, A. Martynov, N. J. Miller, R. F. Mitchell, M. Munoz-Torres, A. Muszewska, Brenda Oppert, S. R. Palli, K. A. Panfilio, Y. Pauchet, L. C. Perkin, M. Petek, M. F. Poelchau, E. Record, J. P. Rinehart, H. M. Robertson, A. J. Rosendale, V. M. Ruiz-Arroyo, G. Smagghe, Z. Szendrei, E. M. Szuter, G. W. C. Thomas, A. S. Torson, I. M. Vargas Jentzsch, M. T. Weirauch, A. D. Yates, G. D. Yocum, J-S Yoon, Stephen Richards. 2018. A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Scientific Reports 8: 1931. IF = 4.26, R = 10 out of 64 in Multidisciplinary Sciences.</li> </ol> <ol start="10"> <li>Izzo, V., Y. H. Chen, S. D. Schoville, C. Wang, D. J. Hawthorne. 2018. Origin of pest lineages of the Colorado potato beetle, Leptinotarsa decemlineata. Journal of Economic Entomology. IF = 1.82, R = 17 out of 93 in Entomology.</li> </ol> <ol start="11"> <li>Jones, A., C.J. Mason, G.W. Felton and K. Hoover. 2019. Host plant and population source drive diversity of microbial gut communities in two polyphagous insects. Sci. Reports, in press.</li> </ol> <ol start="12"> <li>Mason, C.J., D. Long, R. Lindroth and K. Hoover. 2019. Asymmetric utilization of host plants by adult and juvenile conspecific cerambycids is related to intra-plant variation in chemical defenses and resource partitioning. Journal of Animal Ecology, (in revision).</li> </ol> <ol start="13"> <li>Wei, J., Q. Zhou, L. Hall, A. Myrick, K. Hoover, K. Shields and T. C. Baker. 2018. Olfactory sensory neurons of the Asian longhorned beetle, Anoplophora glabripennis, specifically responsive to its two aggregation-sex pheromone components. Journal of Chemical Ecology 44(7), 637-649.</li> </ol> <ol start="14"> <li>Mason, C.J., A.M. Campbell, E.D. Scully and K. Hoover. 2018. Bacterial and fungal midgut community dynamics and transfer between mother and brood in the Asian longhorned beetle (Anoplophora glabripennis), an invasive xylophage. Microbial Ecology https://doi.org/10.1007/s00248-018-1205-1</li> </ol> <ol start="15"> <li>Pan, Q., I. Shikano, K. Hoover, T.-X. Liu, and G.W. Felton. 2018. Enterobacter ludwigii, isolated from the gut microbiota of Helicoverpa zea, promotes tomato plant growth and yield without compromising anti-herbivore defenses. Arthropod-Plant Interactions https://doi.org/10.1007/s11829-018-9634-9.</li> </ol> <ol start="16"> <li>Shikano, I., Q. Pan, K. Hoover, and G.W. Felton. 2018. Herbivore-induced defenses in tomato plants enhance the lethality of the entomopathogenic bacterium, Bacillus thuringiensis var. kurstaki. Journal of Chemical Ecology 44: 946-956.</li> </ol> <ol start="17"> <li>Shikano, I., E.M. McCarthy, J.M. Slavicek and K. Hoover. 2018. Jasmonic acid-induced plant defenses delay caterpillar developmental resistance to a baculovirus: Slow-growth, high-mortality hypothesis in plant–insect–pathogen interactions, Journal of Invertebrate Pathology 158: 16-23.</li> </ol> <ol start="18"> <li>Scully, E.D., Mason, C., J. Carlson, M. Tien, and K. Hoover. 2018. Host-plant induced changes in microbial community structure and midgut gene expression in an invasive polyphage (Anoplophora glabripennis). Scientific Reports, DOI: 10.1038/s41598-018-27476-0.</li> </ol> <ol start="19"> <li>Wei, J., Q. Zhou, L. Hall, A. Myrick, K. Hoover, K. Shields and T.C. Baker. 2018. Olfactory sensory neurons of the Asian longhorned beetle, Anoplophora glabripennis, specifically responsive to its two aggregation-sex pheromone components. J Chem. Ecol., 44(7), 637-649.</li> </ol> <ol start="20"> <li>Wang, J., M. Yang; Y. Song; F.E. Acevedo; K. Hoover; R. Zeng; G.W. Felton. 2018. Gut-associated bacteria of Helicoverpa zea indirectly trigger plant defenses in maize. J Chem Ecol https://doi.org/10.1007/s10886-018-0970-0.</li> </ol> <ol start="21"> <li>Tan, C.-W., M. Peiffer, K. Hoover, C. Rosa, F. E. Acevedo, G. W. Felton. 2018. Symbiotic polydnavirus of a parasite manipulates caterpillar and plant immunity. Proceedings of the National Academy of Sciences. 201717934; DOI: 10.1073/pnas.1717934115.</li> </ol> <ol start="22"> <li>Rering C, Beck JB, Vannette RL, Willms SD. Quantitative assessment of nectar microbe-produced volatiles. Role of Natural Products for Biorational Pesticides in Agriculture. ACS. Book Chapter</li> </ol> <ol start="23"> <li>Vannette RL and Fukami T, Contrasting effects of yeast and bacteria on floral nectar traits, Annals of Botany, 121 (7), 1343-1349 </li> </ol> <ol start="24"> <li>Rering C.C, Beck J.J., Hall, G., McCarthy, M., Vannette RL, 2018 Nectar-inhabiting microorganisms influence nectar volatile composition and attractiveness to a generalist pollinator. New Phytologist doi: 10.1111/nph.14809.</li> </ol> <ol start="25"> <li>Mittelbach, M. & Vannette RL. Mutualism in yeasts. Springer edited edition of Biodiversity and Ecophysiology of Yeasts. In press.</li> </ol> <ol start="26"> <li>Beck JJ, Torto B & Vannette RL. 2017 Eavesdropping on Plant-Insect-Microbe Chemical Communications in Agricultural Ecology: A Virtual Issue on Semiochemicals, Journal of Agricultural and Food Chemistry. 65 (25): 5101-5103.</li> </ol> <ol start="27"> <li>Rering C, Beck JB, Vannette RL, Willms SD. Quantitative assessment of nectar microbe-produced volatiles. Role of Natural Products for Biorational Pesticides in Agriculture. ACS. Book Chapter</li> </ol> <ol start="28"> <li>Vannette RL and Fukami T, Contrasting effects of yeast and bacteria on floral nectar traits, Annals of Botany, 121 (7), 1343-1349. </li> </ol> <ol start="29"> <li>Rering C.C, Beck J.J., Hall, G., McCarthy, M., Vannette RL, 2018 Nectar-inhabiting microorganisms influence nectar volatile composition and attractiveness to a generalist pollinator. New Phytologist doi: 10.1111/nph.14809.</li> </ol> <ol start="30"> <li>Mittelbach, M. & Vannette RL. Mutualism in yeasts. Springer edited edition of Biodiversity and Ecophysiology of Yeasts. In press.</li> </ol> <ol start="31"> <li>Beck JJ, Torto B & Vannette RL. 2017 Eavesdropping on Plant-Insect-Microbe Chemical Communications in Agricultural Ecology: A Virtual Issue on Semiochemicals, Journal of Agricultural and Food Chemistry. 65 (25): 5101-5103. </li> </ol> <ol start="32"> <li>Rodriguez- Saona, C., Cloonan, K.R., Sanchez-Pedraza, F., Zhou, Y., Giusti, M.M., and Benrey, B. 2019. Differential susceptibility of wild and cultivated blueberries to an invasive frugivorous pest. J. Chem. Ecol. DOI: 10.1007/s10886-018-1042-1.</li> </ol> <ol start="33"> <li>Klick, J., Rodriguez-Saona, C.R., Hernández Cumplido, J., Holdcraft, R.J., Urrutia, W.H., da Silva, R.O., Borges, R., Mafra-Neto, A., and Seagraves, M.P. 2019. Testing a novel attract-and-kill strategy for Drosophila suzukii (Diptera: Drosophilidae) management. J. Insect Sci. 19(1): 3; 1–6 doi: 10.1093/jisesa/iey132.</li> </ol> <ol start="34"> <li>Pradit, N., Mescher, M.C., De Moraes, C.M., Wang, Y., Vorsa, N., and Rodriguez-Saona, C. Phytoplasma infection of cranberries benefits non-vector phytophagous insects. Frontiers in Ecology and Evolution‒Chemical Ecology. Submitted. </li> </ol> <ol start="35"> <li>S Xu, CJ Liao, N Jaiswal, S Lee, DJ Yun, SY Lee, M Garvey, I Kaplan, T Mengiste.Tomato PEPR1 ORTHOLOG RECEPTOR-LIKE KINASE1 Regulates Responses to Systemin, Necrotrophic Fungi, and Insect Herbivory. The Plant Cell 30 (9), 2214-2229</li> </ol> <ol start="36"> <li>U Vidal‐Gomez, C Rodriguez‐Saona, I Kaplan. Constitutive exposure to the volatile methyl salicylate reduces per‐capita foraging efficiency of a generalist predator to learned prey associations. Entomologia Experimentalis et Applicata 166 (8), 661-672</li> </ol> <ol start="37"> <li>LL Ingwell, DA Avila-Ruiz, R Foster, I Kaplan.Tailoring insect biocontrol for high tunnels. Biological Control 123, 76-86</li> </ol> <ol start="38"> <li>TJ Wood, I Kaplan, Z Szendrei. Wild bee pollen diets reveal patterns of seasonal foraging resources for honey bees. Frontiers in Ecology and Evolution 6, 210</li> </ol> <ol start="39"> <li>I Kaplan, A Pineda, M Bezemer. Application and Theory of Plant–Soil Feedbacks on Aboveground Herbivores. I Kaplan, A Pineda, M Bezemer. Aboveground–Belowground Community Ecology, 319-343</li> </ol> <ol start="40"> <li>KS Ingerslew, I Kaplan. Distantly related crops are not better rotation partners for tomato. Journal of Applied Ecology 55, 2506-2516 </li> </ol> <ol start="41"> <li>G Angelella, V Nalam, P Nachappa, J White, I Kaplan. Endosymbionts differentially alter exploratory probing behavior of a nonpersistent plant virus vector.  Microbial Ecology 76, 453-458</li> </ol> <ol start="43"> <li>X Li, M Garvey, I Kaplan, B Li, J Carrillo. Domestication of tomato has reduced the attraction of herbivore natural enemies to pest‐damaged plants. Agricultural and Forest Entomology 20, 390-401</li> </ol> <ol start="44"> <li>Hiltpold I, Hibbard BE (2018) Indirect root defenses cause induced fitness costs in Bt-resistant western corn rootworm. 111:2349-2358. doi:10.1093/jee/toy220.</li> </ol> <ol start="45"> <li>Hiltpold I, Shriver WG (2018) Birds bug on indirect plant defenses to locate insect prey. 44:576-579. doi:10.1007/s10886-018-0962-0 </li> </ol> <ol start="46"> <li>Johnson SN, Glauser G, Hiltpold I, Moore BD, Ryalls JMW (2018) Root herbivore performance suppressed when feeding on a jasmonate-induced pasture grass. 43:547-550. doi:10.1111/een.12527</li> </ol> <ol start="47"> <li>Schumann M, Ladin ZS, Beatens JM, Hiltpold I (2018) Navigating on a chemical radar: Usage of root exudates by foraging Diabrotica virgifera virgifera larvae. 142:911–920. doi:10.1111/jen.12480 </li> </ol> <ol start="48"> <li>Truitt, L. L., S. H. McArt, A. H. Vaughn and S. P. Ellner. Trait-based modeling of multi-host pathogen transmission: Plant-pollinator networks. In press at American Naturalist.</li> </ol> <ol start="49"> <li>Adler, L. S., K. Michaud, S. P. Ellner, S. H. McArt, P. C. Stevenson and R. E. Irwin. 2018. Disease where you dine: Plant species and floral trait variation in pathogen transmission to bumble bees. Ecology 99:2535-2545.</li> </ol> <ol start="50"> <li>Tumminello, G., T. A. Volk, S. H. McArt and M. K. Fierke. 2018. Maximizing pollinator diversity in willow biomass plantings: A comparison among willow sex and pedigrees. Biomass & Bioenergy 117:124-130.</li> </ol>

Impact Statements

Grants Received: As a group we have been very successful in funding(~$5,000,000 total). McArt (PI): “Ecological and economic benefits of pollinator-friendly wildflower plantings on solar sites in New York” Cypress Creek Renewables, Inc., $99,998; Jander (PI), McArt (Co-PI): “Plant biotic interactions in agricultural systems” USDA NIFA REEU $272,719 ; McArt (PI), Danforth, McFrederick & Baert (co-PIs): “Fungicides and pollinator health: Quantifying mechanisms of stress to inform real world solutions” 499,000;Adler (PI) “Elucidating mechanisms underlying the medicinal effects of sunflower pollen on bee pathogens.” USDA-NIFA 500,000; Chen (PI) “Evaluating the role of epigenetics in the evolution of insecticide resistance” USDA AFRI SEED $199,947; Hoover (PI) “Detection and Impacts of Spotted Lanternfly on Tree Health in Pennsylvania Forests” USDA-NIFA McIntire-Stennis $200,000; Hoover (PI) “Spotted lanternfly host preference, dispersal patterns in forested landscapes, and impacts on tree health “ USDA Forest Service, State & Private Forestry 39,183; Hiltpold (PI) “Control of slugs in a multi-trophic context: Using friends to manage foes” Delaware soybean Board $7,194; Whitehead (PI) “Pest management practices can impact the apple microbiome with downstream consequences for insect resistance, fruit quality, and human health” USDA-NIFA $500,000; Vannette (PI) “Evaluating Epilobium canum cultivars for floral traits and attraction of beneficials” Saratoga Horticulture Research Endowment Award $19,890; Vannette (PI) “Sustainable Microbial Control of Blossom Brown Rot Blossom Blight in Almond” Almond Board of California $84,000; Thaler (PI) “Using Colorado potato beetle responses to predators to maximize pest control” USDA-NIFA $489,107; Rodriguez-Saona (Co-PI) “Furthering the development and implementation of systems-based organic management strategies for spotted wing drosophila” USDA-OREI $145,000; Rodrigez-Saona (PI) “Spotted wing drosophila/blueberries- attract and kill” IR-4 Biopesticide Grants. IR-4 Minor Crop Pest Management Program $26,000; Ali (PI), "Consequences of host plant toxicity across monarch butterfly ontogeny: milkweed challenges from feeding to flying," NSF $897,841.00; Ali (Co-PI) “Solutions for managing Allium leafminer: a new invasive threat to Allium crops in North America” USDA NIFA $325,000; Ali (Co-PI) “Impact of Spotted Lanternfly on Quality of Pennsylvania Wines”. Pennsylvania Department of Agriculture, Wine Marketing aand research Program $50,000; Ali (PI) "Cover crop cascades can benefit mycorrhizae-associated maize resistance to insect pests," USDA NIFA $500,000.

Date of Annual Report: 01/20/2020

Report Information

Annual Meeting Dates: 10/17/2019 - 10/18/2019
Period the Report Covers: 01/01/2019 - 01/01/2020

Participants

Meeting Participants

Jared Ali, Penn State
John Tooker, Penn State
Sara Hermann, Penn State
Anurag Agrawal, Cornell
Jennifer Thaler, Cornell
Susan Whitehead, Virginia Tech
Will Wetzel, Michigan State
Cesar Rodriguez-Soana, Rutgers
Tom Baker, Penn State
Jim Tumlinson, Penn State
Tanya Renner, Penn State
Kelli Hoover, Penn State

Brief Summary of Minutes

Brief Summary of Minutes of Annual Meeting

The group met on October 17-18th, 2019 on the Pennsylvania State University campus in University Park, PA. We had 12 participants attending the meeting that was led and organized by Jared Ali. We had many first time participants. Our goal was to discuss the next directions for the group and how they impact sustainable management practices in the Northeast. To this end, we had a specific theme for this meeting: “Defining new goals of chemical ecology for sustainable pest management”. The day was structured into two sessions The first session comprised of talks by each PI geared to touch on the following three topics: A) Talk about how your research has made an applied contribution with specific discussion of what the key features lead to this success, B) Discuss a result you have that you think could be applied, point out what you think the stumbling blocks to application are and get feedback on making this jump, and C) Discuss a totally fundamental idea that you think people with an applied focus should be taking into consideration. In the second session we had a larger group discussion on how we should structure the resubmission of the hatch project and what major themes should be included.

The executive decisions that were made during this meeting were:

That the next organizational meeting is going to be organized at Cornell University (unless after polling the members not present, via emai,l have an alternative suggestion) and it will be taking place in Fall 2020.

That the chair of the Executive Committee for the next year was going to be Andre Kessler, with representative at large and the secretary to be decided.

We decided to re-submit our hatch project for consideration.

MEETING MINUTES (summary of main results and points discussed)

General Topic of this year’s meeting and talk format: “Turning our biological discoveries into useful applications”

1) Morning session

Talks per PI on the following:

Talk about how your research has made an applied contribution with specific discussion of what the key features lead to this success

Talk about a result you have that you think could be applied, point out what you think the stumbling blocks to application are and get feedback on making this jump

Have a totally basic idea that you think people with an applied focus should be taken into consideration

2) Afternoon Discussions

Large group brain storming led by Jennifer to outline the resubmission goals.

Agenda

Thursday: 6 pm group dinner

Friday meeting the “MorningStar Solar Home”

9:30 coffee & Bagels

9:45 Welcome & Introductions

10:05- 11:05: Short intro talks (Cesar, Jennifer, John, Jared, Jim, Will, Sar)

11.05-11:15: break

11:15-12:15: Short intro talks (Tom, Tanya, Rose, Anurag, Kelli, Susan, Flor)

12:15-1:15: Lunch

1:15- 1:25: Group photo

1:30-2:00: Discussing the renewal

2:00-2:45: Topical Research Brainstorming

2:45-3:30: Reconvene

3:30-4:15: Topical Research Brainstorming

4:15-5:00: Reconvene and goals (Annual report, choosing next leadership, next meeting time and location, renewal process)

6pm Dinner

Accomplishments

Outputs: The most significant outputs have been the writing of research proposals based on preliminary data gathered since the establishment of this multistate project. New funded projects that originated from this multistate include projects concerned with the conservation of monarch butterflies, through a better understanding of the interactions with milkweeds; projects investigating the trade-offs between crop protection and pollination services have been initiated that involve PI’s with expertise in pollination, agricultural economics, crop protection, landscape ecology and agroecology; work utilizing indirect predator- prey interactions to protect crops; and a project looking at how the apple microbiome has downstream consequences for insect resistance. Manuscripts have been submitted and published during this time (for details see impact statement below). Most PI’s involved in this multistate have also disseminated their results at national conferences like the Ecological Society of America, Gordon Research Conferences, International Society for Chemical Ecology and the Entomological Society of America meeting. PI’s have also interacted with farmers, and other stakeholders such a beekeepers and crop breeders, to start establishing means by which the performed research can be translated to tools and management strategies to protect pollinators, reduce pest pressure and increase yields. Activities/Milestones: This year, Michael Stout’s group focused on the possibility that treating rice seeds with methyl jasmonate could protect rice from pest herbivores by inducing resistance in plants was tested in small-plot field trials in 2017 and 2018.Treatments applied to plots were factorial combinations of 2.5 mM methyl jasmonate (applied by soaking seeds) and repeated applications of a pyrethroid insecticide.  Results showed that methyl jasmonate seed treatments reduced populations of the rice water weevil (Lissorhoptrus oryzophilus) almost as effectively as insecticide applications. Methyl jasmonate treatments also reduced plant emergence and plant biomass and delayed heading.  Yields, however, did not appear to be reduced. The effect of methyl jasmonate seed treatments on rice plant yields were further investigated in a greenhouse environment lacking pests in 2019, and again no significant effect on plant yield was observed (although plant growth was again reduced).  Thus, treatment of rice seeds with methyl jasmonate may be an effective tool for reducing populations of early-season pests in rice. The results of the field experiments conducted in 2017 and 2018 were published in a refereed journal in fall of 2019. An additional project conducted by an undergraduate investigated the combined effects of low doses of Bt toxins (Cry1Ac) and resistant maize varieties against fall armyworm.  Several putatively resistant and susceptible maize lines (obtained from X. Ni, USDA-ARS, Tifton, GA) were tested and experiments have nearly been completed. The effects of plant resistance and Bt toxin on armyworm growth and mortality were found to be mostly independent of one another; little evidence of synergism or antagonism was found. Another set of experiments has been initiated to characterize the volatiles emitted by rice panicles at several stages of development and to determine which of the volatiles are involved in attraction of rice stink bugs to panicles. To this point, a series of behavioral assays have shown that rice stink bugs prefer to feed on panicles in the milk stage of grain development, and that they may be attracted to previously injured panicles over uninjured panicles. Over the past year the group lead by Scott McArt accomplished several of their multi-state chemical ecology project goals. This year of the project focused on initiating and staffing a multi-residue pesticide detection facility at Cornell that’s available to all multi-state colleagues. This resulted in a facility that can currently quantify 270 pesticides in range of matrices (pollen, flowers, bees, soil, etc.). Next, field experiments focused on understanding co-occurring pesticide exposures to honey bees, bumble bees, and other wild bees during strawberry pollination. Finally, laboratory experiments tested whether common co-occurring exposures resulted in additive or synergistic toxicity to bees. The field and laboratory work is ongoing. In addition to making the multi-residue pesticide facility available to researchers and the public, we have published 1 peer-reviewed paper, 2 pesticide decision-making extension guides, used data from the project to leverage 1 USDA NIFA grant, and have 3 manuscripts in preparation. The Adler lab has made significant progress in pollinator health. They have published our original findings that sunflower pollen reduced Crithidia in B. impatiens, reduced Nosema in Apis mellifera, and that more sunflower acreage was associated with lower Crithidia infection in wild-caught B. impatiens. They’ve has a manuscript that demonstrates that pollen from many cultivated sunflower cultivars, wild populations, two congeners, and Solidago, a distant relative in the same family, all reduce Crithidia in B. impatiens relative to buckwheat pollen, and most relative to sunflower pollen (LoCascio et al in review). Their other manuscript, which should be submitted in the next month, asks how timing of exposure to sunflower pollen during foraging or after infection affects Crithidia infection in B. impatiens. They’ve found that exposure to sunflower pollen during foraging does not influence infection, but the timing and duration of sunflower pollen after inoculation both affect infection outcomes. Their research is allowing them to identify whether and under what conditions sunflower supplements could be developed and marketed for commercial bumble or honey bee rearing. So far, results seem more promising with bumble than honey bees.  Yolanda Chen and her research group has meet a major accomplishment this past year. They studied the beetle genome for evidence of genomic features that could contribute to the beetle’s ability to evolve rapidly. Transposable elements contribute to least 17% of the beetle’s highly fragmented genome, suggesting that they may be a larger portion of a completed genomes. We found that the beetle has expansions in gene expansions in digestive enzymes and gustatory receptors. However, contrary to our expectations, CPB does not show expansions in gene families associated with detoxification. We have also found that CPB ranks as one of the fastest to evolve resistance to insecticides. We also published a phylogeographic history study on CPB showing that the pest populations are derived from plains beetles, and beetles in the southwestern US are more similar to Mexico. Finally, we also published a conceptual paper on transgenerational effects of insecticides, as part of a special issue in Current Opinion in Insect Science titled, “Ecological Adaptation in Agroecosystems”. Kelli Hoover’s group completed studies on impact of phenolic glycosides on Asian longhorned beetle; began studies on pollinator deficiency of black cherry in Pennsylvania; began studies on plant-insect interactions and the requirement for tree-of-heaven for development of spotted lanternfly (SLF) on woody ornamentals and in forest systems. They determined that there is resource partitioning by Asian longhorned beetle and adults on poplars in response to high levels of phenolic glycosides in bark (fed on by adults), but not wood (fed on by larvae). The group also demonstrated that the fungal gut symbiont of ALB is transmitted from mother to offspring during oviposition. In addition, they documented that lepidopterans feeding on the same host plant in the same part of the plant and the same field harbor different gut microbial communities, likely due to an environment X genetic interaction. Lastly, they figured out how to rear spotted lanternfly under greenhouse conditions in quarantine; also set up field experiment with planted trees in replicated plots in SLF quarantine zone to investigate differences in SLF performance on different host plants.  Work in Susan Whitehead’s lab is relevant to two of the major goals of the multistate project: (1) Develop chemical ecology tools and information to support sustainable agriculture by reducing damage by pests in crops such as potatoes, brassicas, cucurbits, apples, blueberries, and sweet corn, while maintaining pollinator health in agricultural systems, and (2) Assess the impact of domestication on plant and animal chemical ecology in agricultural fields and identify unifying patterns of human and natural selection on chemical interactions of crop plants.We focus on apples as a model system to address these goals. Apples produce a diversity of both volatile and non-volatile secondary metabolites that could function in defense, but their effects on herbivores and natural enemies are almost entirely unexplored. Furthermore, nothing is known about how apple chemical defenses may have been altered during domestication. Our research this year focused on chemical analyses and integrating and analyzing data from past experiments to examine: 1) how apple fruit chemistry mediates resistance to fruit-feeding insects, 2) how fruit chemistry changes in response to insect feeding, and 3) how fruit chemistry has changed during apple domestication. Given that insecticides cost US farmers over $4.3 billion annually, understanding and harnessing natural fruit defenses could be a promising tool to increase the economic and environmental sustainability of apple production. In this reporting period, Rachel Vannette’s group worked on two projects related to the goal of the multi-state group. Project 1: Microbial communities of floral nectar and effects on chemistry and pollinators.They continued to examine the composition of microbial inhabitants of flowers and their effects on pollinators. Volatile composition of nectar-dwelling microorganisms including 2 fungal species and 2 bacterial species were validated using quantitative methods. This forms an excellent dataset for future manipulative experiments. The effects of microbial volatiles on honey bees was examined. They found that microbial taxa inhabiting nectar produce volatile compounds, that honey bees can detect these compounds, that bees exhibit specific preferences for the volatile blends of particular microbial strains. In particular, the volatiles produced by the nectar yeast Metschnikowia reukaufiiwere distinct and most attractive to honey bees compared to other fungi and bacteria isolated from flowers. They also identified fungal volatiles from field-sampled plants that had high densities of yeasts in floral nectar, suggesting that microbial growth can influence floral scent in field conditions. They screened nearly 50 plant species for abundance of fungi and bacteria in floral nectar. This work is being analyzed and written up. Other related projects also continued. They performed experiments to examine which microbial strains may act as effective antagonists in floral nectar against the pathogen Erwinia amylovoraand identified candidates. They are also performing antagonist trials to examine which floral microbes can suppress the growth of the fungus (Monilinia laxa) that causes blossom blight in almond. Project 2: Effects of soil management on plant chemical defense against pests:They also continued examining how soil management practices influence microbial composition and plant defense. Results were submitted for publication. In summary, They found that organic management significantly influences both bacterial and fungal composition in tomato rhizosphere and are linked to plant defense against phloem-feeders. Judy Wu Smart’s projects aligns with NE1501 objectives @2,3, and 6.To accomplish these objectives, their project goals are as follows: Examine the role existing tree lines play as drift barriers on crop margins to reduce neonicotinoid dust contamination in non-target areas and reduce Bt toxin exposure on butterflies. 2. Assess benefits of in-field options (winter wheat/legume cover crop mix in the corn-soy rotation) in regards to enhanced bee forage via cover crop on bees and on soil quality and corn yields.3. Assess impact of landscape enhancements (pollinator habitat & drift barriers) on pollinator and other beneficial insect community abundance and diversity.4. Evaluate NE farmer willingness to adopt landscape enhancements using surveys and economic modelling and provide opportunities for outreach and educational events and materials (agroecosystem demonstration farms for other growers, 4-H and K-12 groups, Best Management Practices guidelines). The Agrawal group has now completed three studies of crop domestication and their impacts on plant secondary metabolites and resistance to insects herbivores using lettuce, sweet potato, and squash. Work involved collaboration with scientists from NC State as well as California. The lettuce results were more promising, and showed that in multiple cultivars, resistance of lettuce varieties was reduced compared to wild lettuce. However, this effect was reversed when latex was deactivated in plants, likely because of higher nutritive value of wild lettuce leaves (in the absence of latex).  We will conduct some final chemical analyses and work towards publication. Work with squashes was detailed at the multi-state meeting and a paper has been submitted (see below). Briefly, we used two distinct domestication events of Cucurbita pepo to identify mechanisms of reduced preference to the striped cucumber beetle (and the interaction between plant traits and pheromone production). This year, research lead by Jennifer Thaler addressed Objective 2 of the Multistate projectThis year, our research addressed Objective 2 of the Multistate project. Little is known about population variation in predator- prey interactions even though it is critical for understanding how biological control agents will work in different locations. We have been measuring variation in responses to predators between populations of Colorado potato beetles that are resistant or susceptible to insecticides. Colorado potato beetle is well- known for it’s ability to evolve resistance to insecticides, making it a difficult pest to control. In places with a history of intensive insecticide use, resistance has evolved. This may impact interactions with predators because resistant individuals have different behavior and physiology than susceptible individuals. This may impact the effectiveness of biological control agents in populations with resistant individuals. This year, we analyzed the results from the resistant/susceptible populations and began working on writing the manuscript. In addition, we worked on the statistical analysis and writing up the results from the landscape experiment that we conducted in Year 1 of this project looking at how the farm environment affected the prey responses to predators. We found that beetles from farms in low complexity landscapes were more responsive to their predators, suggesting they may be more defended against biocontrol agents.   Katja Poveda has established plots of two varieties of zucchini, one that was more resistant and one more susceptible to striped cucumber beetle summer. Each variety was subjected to different treatments that differed in the way the insecticide was applied to the plant (control, foliar application, seed coating and soil drenching). Soil drenching and seed coating provided the best pest control and reduced leaf damage. They are currently analyzing the results of insecticide residue found in the pollen and nectar to hopefully find insecticide application methods that reduce plant damage and reduce the impact on pollinators.  The group lead by Jared Ali has three projects. i)Cover crops legacy effects on plant resistance to herbivores: With funding from the USDA theyare investigating how multiple management components can be integrated to enhance plant resilience to stressors and improve productivity. We have found that the species of cover crop farmers choose has legacy effects on the subsequent corn crop’s resistance to the European corn borer, and that this legacy is mediated by soil fertility and/or mycorrhizal colonization. The goal of this proposal is to discover mechanisms that control the cascade of interactions linking cover crops, soil fertility, and corn pest management. ii) Using beneficial nematodes to prime plant resistance to pests: In this project we are studying chemical cues that play important roles in ecological interactions, especially among plants and invertebrates. A relatively recent and exciting discovery is that plants perceive and respond to chemical cues, often detecting herbivore-associated cues as a warning to prepare for future attack. Finding novel ways to harness these natural cues and organismal responses for enhancing crop protection represents a new frontier in agroecology. A major goal of this project is to elucidate indirect benefits of EPNs for plant protection against herbivores. iii)Monarchs, migrations and milkweed: We have initiated a pollinator health conservation project linking variation in milkweed defense biochemistry to variation in larval and resulting adult monarch butterfly fitness traits. We are quantifying variation in plant toxicity traits within and across milkweed species using state-of-the-art methods in chemical ecology to determine how plant defense affects larval growth and subsequent adult fecundity, in reproductively active monarch butterfly cohorts. Using a combination of respirometry, flight kinematic analyses, and studies of lipid metabolism, we are examining how milkweed toxicity experienced during larval stages affects adult flight performance and energetics in migratory monarchs and will link these effects to expression of microRNAs controlling traits associated with migratory phenotypes. This project adds a novel perspective to typical chemical ecology practices to studying plant-herbivore interactions by examining physiological consequences of trophic interactions across the entire ontogeny of an herbivorous insect. The project substantially advances the knowledge of the basic biology of the iconic milkweed-monarch butterfly system, a model migratory insect with a complex ecology.   Cesar Rodriguez-Saona lead a number of projects that align with the goals of the multi-state group.Goal 1: They conducted studies on the chemical ecology of the new invasive pest, spotted wing drosophila (SWD). They evaluated an "attract-and-kill" strategies to control SWD known as "HOOK SWD Lure-and-Kill" (ISCA Technologies, Inc.).” We conducted cage studies to assess the effects of SWD density on the efficacy of this attract-and-kill strategy. They determined that the efficacy of HOOK SWD decreases with increasing SWD densities. Goal 2: In previous studies, they determined that phytoplasma infection of cranberries improves nutrient content and reduces defenses, which in turn improved adult mass of insect vectors but reduced their oviposition. Phytoplasma infection also improved non-vector larval mass and consumption. In 2019, they conducted studies on the effects of various commercially-available activators of the salicylic acid (Actigard, Regalia, LifeGard) and jasmonic acid (Blush 2X) defense pathways on vector and non-vector insects. They found that phytoplasma infection interacted with elicitors to affect vector and non-vector differently. In general, all activators of defenses made the plants more susceptible to these insects. Similarly, phytoplasma infection increased plant susceptibility to herbivores regardless of activator treatment. They are currently analyzing the nutrient content, phytohormone and proanthocyanidin levels, and defense gene expression of phytoplasma-infected and uninfected cranberry plants treated with these various defense activators. Goal 3: They evaluated the effects of domestication on plant defenses against herbivores in blueberries. They tested the preference of the new invasive pest, spotted wing drosophila, between wild and domesticated blueberries. Choice experiments were conducted and headspace volatiles were collected and identified. They found that wild berries more attractive to SWD than cultivated berries. We identified four compounds from wild berries that attract SWD.Goal 4: Ongoing research outlined in this project was presented at national and international scientific meetings, including the 2019 Entomological Society of America Annual Meeting (St. Louis, MO), the 2019 International Society of Chemical Ecology (ISCE) Annual Meeting (Atlanta, GA), the 2019 Asia-Pacific Association of Chemical Ecologists (APACE) Meeting (Hangzhou, China), and at annual blueberry and cranberry growers meetings in New Jersey.   Milesstones: As a group we have reached several milestones pertaining to our different objectives. Most activities have been focusing on defining the variability of chemical mediated interactions between pests, crops and beneficial organisms in terms of plants chemistry, species interaction and landscape factors in the Northeast (Objective 2). Here we have an overall better understanding of which chemical cues are mediating interaction between plants and their herbivores, how the landscape is shaping interaction between crops, herbivore pests, and predators, how plant quality can affect pollinator health and how the quality of the crop influence their interactions with herbivores. Regarding our second objective on developing chemical ecology tools and information to support sustainable agriculture by reducing damage by pests in crops such as potatoes, brassicas, cucurbits, apples, blueberries, and sweet corn, while maintaining pollinator health in agricultural systems we have definitively started to identify the main chemical cues that are involved in important interaction between plants and their pests or vectors of important diseases. There are promising tools that can help control Spotted Lanternfly, Spotted Wing Drosophila, while other information could be used as tools for more sustainable agriculture. Our 5th objective of establishing a chemical ecology analytical facility in the Northeast has progressed. By further establishing ties between Cornell's and Pennstate's Chemical ecology Core groups and facilities we have begun to work out funding structures and pipelines to process samples and/or analyze behavior.  The shared expertise among members of this multistate have allowed for the availability of shared equipment across the NE, fulfilling this objective. Training  Several postdocs, technician and PhD students have been trained across these projects with planned travel and cooperation between universities. They are not just receiving training on the chemical ecology of plant interactions and their potential use for sustainable agriculture, but also receiving substantial professional development.  Planned activities for the next year In the coming year, we have planned to resubmit for renewal of the chemical ecology research multi-state network.  Also grant proposals will continue to be written based on preliminary data generated in the course of this multistate.  We will continue developing all proposed objectives, and work on new items in our developing project renewal. All groups that have obtained funding through this multistate will also present the results to the research community at national meetings and will disseminate their work also at local farmer meetings.

Publications

<ol> <li>Iverson, A. L., C. Hale, L. Richardson, O. Miller and S. H. McArt. 2019. Synergistic effects of three sterol biosynthesis inhibiting fungicides on the toxicity of a pyrethroid and neonicotinoid insecticide to bumble bees. Apidologie 50:733-744.</li> <li>Van Dyke, M., E. Mullen, D. Wixted and S. H. McArt. 2018. A pesticide decision-making guide to protect pollinators in landscape, ornamental, and turf management. 36 pp.</li> <li>Van Dyke, M., E. Mullen, D. Wixted and S. H. McArt. 2018. A pesticide decision-making guide to protect pollinators in tree fruit orchards. 31 pp.</li> <li>Bjorklund N., Lamke K., Gupta Vakil S., and Wu-Smart J. (2018) Alfalfa leafcutting bee (Megachile rotundata F.) arthropod pests and management. Pacific Northwest Insect Pest Management Handbook.</li> <li>Mollet K., Gupta Vakil S., and Wu-Smart J. (2018) Alkali bee (Nomia melanderi Ckll.) arthropod pests and management. Pacific Northwest Insect Pest Management Handbook.</li> <li>Lamke K. and Wu-Smart J. (2018) Blue orchard bee (Osmia lignaria Say) arthropod pests and management. Pacific Northwest Insect Pest Management Handbook.</li> <li>Brummel S., Brummel C., Scholl D., and Wu-Smart J. (in review) Getting Honey Certified in Nebraska. Neb Guide Publication.</li> <li>Lamke K., Schacht W., Wedin D., and Wu-Smart J. (in review). Conserving Biodiversity: A Bee’s Role in Prairie Grasslands. Nebraska Extension Circular.</li> <li>Mollet K., Peterson J., Schacht W., and Wu-Smart J. (in review). Pollinator Habitat Program for Public Land Managers in Nebraska. Neb Guide Publication.</li> <li>Chen, J. *, M.J. Stout, J. Beuzelin, T. Smith, D. Labonte, and J.A. Davis. 2019. Host preference of sweetpotato weevil, Cylas formicarius elegantulus (Summers): an example of Hopkins' host-selection principle. Arthropod-Plant Interactions, https://doi.org/10.1007/s11829-019-09704-0.</li> <li>Kraus EC, Stout MJ (2019) Seed treatment using methyl jasmonate induces resistance to rice water weevil but reduces plant growth in rice. PLoS ONE 14(9): e0222800. https://doi.org/10.1371/journal.pone.0222800.</li> <li>Salamanca, J., Brigida Souza. B., Vera Kyryczenko-Roth, V., and Rodriguez-Saona, C. 2019. Methyl salicylate increases attraction and function of beneficial arthropods in cranberries. Insects, Special Issue on “Semiochemicals and Insect Behavior,” 10, 423, doi: 10.3390/insects10120423.</li> <li>Pradit, N., Mescher, M., De Moraes, C., and Rodriguez-Saona, C. 2019. Phytoplasma infection of cranberry affects development and oviposition, but not host-plant selection, of the insect vector Limotettix vaccinii. J. Chem. Ecol. doi: 10.1007/s10886-019-01137</li> <li>Brzozowski, L.J., J. Gardner, M.P. Hoffmann, A. Kessler, A.A. Agrawal, M. Mazourek. (in review) Attack and aggregation of a major squash pest: parsing the role of plant chemistry and beetle pheromones.Ecological Entomology.</li> <li>Schaeffer RN, C Rering, I Maalouf, JJ Beck, Vannette RL, Microbial metabolites elicit distinct olfactory and gustatory preferences in bumblebees, Biology Letters 15 (7), 20190132.</li> </ol> <ol start="16"> <li>Schmidt, JE, Igwe AI, Blundell R, Gaudin A, Casteel, C, Vannette RL, “Effects of agricultural management on rhizosphere microbial structure and function in processing tomato” Applied and Environmental Microbiology, AEM. 01064-19.</li> </ol> <ol start="17"> <li>Lee, C*. Tell L, T Hilfer*, Vannette RL. 2019. Microbial communities in hummingbird feeders are distinct from floral nectar and influenced by bird visitation. Proc R Soc B. 286 (1898), 20182295.</li> <li>Zemenick, A., Rosenheim, J, Vannette RL. Legitimate visitors and nectar robbers of Aquilegia formosa have different effects on nectar bacterial communities , Ecosphere e02459.</li> </ol> <ol start="19"> <li>Rering C, Beck JB, Vannette RL, Willms SD. Quantitative assessment of nectar microbe-produced volatiles. Role of Natural Products for Biorational Pesticides in Agriculture. ACS. Book Chapter</li> <li>Blundell, R, Schmidt JE, Igwe AI, Cheung AL, Vannette RL, Gaudin A, Casteel, C “Organic management promotes natural pest control through enhanced plant resistance to insects”, in revision and at biorxiv https://www.biorxiv.org/content/10.1101/787549v1</li> <li>Zemenick, A. Vannette RL, Rosenheim J. Floral visitation networks shape plant-microbe interactions, on biorxiv https://www.biorxiv.org/content/10.1101/847376v1.abstract</li> <li>Davidson-Lowe, E., Szendrei, Z., & Ali, J. (2019). Asymmetric effects of a leaf-chewing herbivore on aphid population growth. ECOLOGICAL ENTOMOLOGY, 44(1), 81-92. </li> </ol> <ol start="23"> <li>Stelinski, L. L., Willett, D., Rivera, M. J., & Ali, J. (2019). ‘Tuning' communication among four trophic levels of the root biome to facilitate biological control. BIOLOGICAL CONTROL., 131, (pp. 49-53). </li> </ol> <ol start="24"> <li>Helms, A. M., Ray, S., Matulis, N. L., Kuzemchak, M. C., Grisales, W., Tooker, J. F., & Ali, J. (2019). Chemical cues linked to risk: Cues from below-ground natural enemies enhance plant defences and influence herbivore behaviour and performance. FUNCTIONAL ECOLOGY, 33(5), 798-808.</li> </ol> <ol start="25"> <li>Paudel, S., Lin, P.-A., Foolad, M. R., Ali, J., Rajotte, E. G., & Felton, G. (2019). Induced Plant Defenses Against Herbivory in Cultivated and Wild Tomato. JOURNAL OF CHEMICAL ECOLOGY, 45(8), 693-707.</li> <li>Markovic, D., Colzi, I., Taiti, C., Ray, S., Scalone, R., Ali, J., Mancuso, S., & Ninkovic, V. (2018). Airborne signals synchronize the defenses of neighboring plants in response to touch. JOURNAL OF EXPERIMENTAL BOTANY, 70(2), 691-700.</li> <li>Ray, S., Helms, A. M., Matulis, N. L., Davidson-Lowe, E., Grisales, W., & Ali, J. G. (2019). Asymmetry in Herbivore Effector Responses: Caterpillar Frass Effectors Reduce Performance of a Subsequent Herbivore. Journal of Chemical Ecology, 1-8.</li> </ol>

Impact Statements

Grants Received: As a group we have been very successful in funding in 2019(~$3,000,000 total). Wu-Smart(PI) “The Great Plains Regional Training For Beginning Beekeeping Farmers” USDA-NIFA Beginning Farmer Rancher Development Program $393,322; Agrawal(PI) Cucumber’s Cucurbitacins: Impacts on Beetles, Pollinators and Disease” Hatch / Federal Formula Funds $105,000; Vannette (PI) “ Effects of soil management on processing tomato associations with mycorrhizal fungi” California Tomato Research Institute, $33,998;Vannette (PI) “Screening potential antagonists for fire blight control” Pear Pest Management Research Fund, $15,000; Vannette(PI) “Characterizing the structure and function of pollination microbiomes” Hellman Fellowship Award $25,000; Vannette (PI) “Sustainable Microbial Control of Blossom Brown Rot Blossom Blight in Almond” Almond Board of California, $84,000; Vannette (PI) “Nectar chemistry and ecological and evolutionary tradeoffs in plant adaptation to microbes and pollinators”, National Science Foundation $896,057;Vannette (Co-PI) “The brood cell microbiome of solitary bees: origin, diversity, function, and vulnerability” National Science Foundation, $297,335; Ali (PI)” Harnessing multi-trophic chemical ecology to obtain sustainable pest control and improved soil health” Foundation for Food and Agricultural Research, $600,000; McArt(PI) “Fungicides and pollinator health: Quantifying mechanisms of stress to inform real world solutions” USDA NIFA $499,000