Brief Summary of Minutes of Annual Meeting

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.

1.      Talk about how your research has made an applied contribution with specific discussion of what the key features lead to this success
2. 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
3. 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)

Activities/Milestones:

• 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.

• 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. 

• 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.

• 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”.

• 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 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.

• 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.

• 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.

• 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.

• 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.

• 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).

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 5^th 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.

1. 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

2. 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

3. 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 

4. 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.

5. 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

6. 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.

7. 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.

8. 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

9. 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.

10. 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.

11. 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.

12. 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).

13. 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.

14. 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

15. 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.

16. 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.

17. 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.

18. 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.

19. 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.

20. 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.

21. 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.

22. 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

23. Vannette RL and Fukami T, Contrasting effects of yeast and bacteria on floral nectar traits, Annals of Botany, 121 (7), 1343-1349 

24. 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.

25. Mittelbach, M. & Vannette RL. Mutualism in yeasts. Springer edited edition of Biodiversity and Ecophysiology of Yeasts. In press.

26. 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.

27. 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

28. Vannette RL and Fukami T, Contrasting effects of yeast and bacteria on floral nectar traits, Annals of Botany, 121 (7), 1343-1349. 

29. 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.

30. Mittelbach, M. & Vannette RL. Mutualism in yeasts. Springer edited edition of Biodiversity and Ecophysiology of Yeasts. In press.

31. 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. 

32. 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.

33. 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.

34. 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. 

35. 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

36. 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

37. LL Ingwell, DA Avila-Ruiz, R Foster, I Kaplan.Tailoring insect biocontrol for high tunnels. Biological Control 123, 76-86

38. 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

39. 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

40. KS Ingerslew, I Kaplan. Distantly related crops are not better rotation partners for tomato. Journal of Applied Ecology 55, 2506-2516 

41. 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

43. 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

44. 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.

45. 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 

46. 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

47. 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 

48. 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.

49. 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.

50. 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.