Source: PENNSYLVANIA STATE UNIVERSITY submitted to NRP
THE CHEMICAL ECOLOGY OF INTERACTIONS AMONG PLANTS, INSECTS AND MICROORGANISMS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
HATCH
Reporting Frequency
Annual
Accession No.
0229574
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Jul 1, 2012
Project End Date
Jun 30, 2016
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
PENNSYLVANIA STATE UNIVERSITY
208 MUELLER LABORATORY
UNIVERSITY PARK,PA 16802
Performing Department
Entomology
Non Technical Summary
The world currently faces an array of complex environmental challenges. Among the most pressing of these is to sustain and increase our capacity for food production in order to meet increasing demand without irreversible damage to ecological and other natural resources. Beginning more than 50 years ago, the so- called green revolution harnessed the power of science to develop modern agricultural techniques for plant breeding, weed and pest control, irrigation, and fertilization that greatly increased the human capacity for food production in both industrialized and non-industrialized nations. Yet this revolution remains incomplete if our goal is to reliably and sustainably feed a growing world population that many demographic experts believe will reach 12.5 billion by 2050. Population growth, changing demographics, and unceasing poverty, together with unsustainable use of chemical inputs have already overtaken many of the initial gains of the green revolution. If the gains of the green revolution are to be consolidated and advanced, researchers and farmers worldwide face the challenge of developing and applying technology that can increase crop yields by 50-75 percent over the next 25 years, and doing so in ways that are economically and environmentally sustainable. Given limitations on the further expansion of agricultural capacity through application of the techniques that initially sparked the green revolution, the development of new agricultural technologies is of primary importance. Our research focuses on understanding the ecological and biochemical bases of plant chemical communication, insect pheromonal communication, and induced-plant defenses. These complex systems hold tremendous potential for the development of new crop protection techniques because plant volatiles are both major determinants of the effectiveness of herbivore natural enemies and important environmental cues used by herbivores, which damage plants directly as well as vectoring many important plant diseases. Moreover, understanding insect pheromone signaling may allow insect control tactics to exploit or short-circuit this vital line of information sharing between the sexes of pest species. Increased understanding of these systems will eventually allow us to influence their dynamics at levels ranging from the molecular to the ecological. Importantly, we have active efforts to clarify the pest management potential some of the basic research our project is developing. There is little doubt that the need for new, ecologically sustainable methods of pest management is profound, requiring a fundamental shift in our thinking about the management of agricultural systems. Effective and lasting solutions to the problems posed by insect can only be achieved by understanding mechanisms governing dynamics of pest populations as part of an integrated ecological system. We must understand and exploit the inherent strengths of the natural system to maintain pest populations below economic thresholds and prevent outbreaks. Understanding the tritrophic interactions among plants, herbivorous insects, and entomophagous insects will be key to such efforts.
Animal Health Component
20%
Research Effort Categories
Basic
80%
Applied
20%
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2111599113060%
2121429113020%
2161599113020%
Knowledge Area
212 - Pathogens and Nematodes Affecting Plants; 211 - Insects, Mites, and Other Arthropods Affecting Plants; 216 - Integrated Pest Management Systems;

Subject Of Investigation
1599 - Grain crops, general/other; 1429 - Cucurbits, other;

Field Of Science
1130 - Entomology and acarology;
Goals / Objectives
1. Clarify and document the role of plant volatiles in chemical communication within and between plant species. 2. Elucidate the role of plant volatiles in plant-pathogen-vector relationships and subsequent effects on disease transmission dynamics 3. Document the effects of population genetic variation on plant volatile production. 4. Identify the individual and combined effects of elicitors present in insect regurgitant on insect-induced plant volatiles. 5. Develop technologies that employ plants in remote sensing of environmental information. 6. Identify environmental conditions that affect plant biochemical changes elicited by insect herbivores on both direct and indirect plant defenses. 7. Develop improved agricultural production techniques, new crop varieties, and intraspecific mixtures that enhance plant resistance to pests, pathogens, and environmental stressors. 8. Understand the influence of sub-lethal doses of herbicides on insect populations and plant-insect interactions. 9. Determine the existence of pheromone communication systems in target insect species and isolate and identify these pheromones for use in detection, monitoring, and mating disruption. 10. Identify and evaluate chemicals that regulate or influence behaviors, including foraging, mating and oviposition, of important beneficial and pest insects. 11. Determine physiological and biochemical mechanisms, elicitors, and regulators involved in the interactions of plants with insect herbivores, their natural enemies, and microorganisms.
Project Methods
Manipulative laboratory and field experiments will be conducted to understand the role of host plant volatiles and semiochemicals in species and trophic interactions. Experiments will span plant-plant, insect-insect, and plant-insect interactions. Mechanistic experiments will involved volatile collections from plants and insects, analytical chemistry, and assays of the influence volatile host-plant compounds and semiochemicals on molecular and physiological status of the plants and insects involved. Results will be interpreted using appropriate statistical analyses and within the context of existing literature, and presented in peer-reviewed publications and at scientific meetings. The proposed research is interdisciplinary by nature, bridging the physical and life sciences and thus readily provides opportunities for student researchers to learn to draw on concepts from both fields. Moreover, this project has strong potential to be used for educational purposes both in formal courses and extension audiences for growers, and outreach programs aimed at a wider audience. This research serves as the basis for a workshop several of us have put on to the Women in the Sciences & Engineering Summer Camp, which teaches students the basics of ecology while providing hands-on experience with the techniques and challenges of field research. We are also involved in a number of other outreach activities including the Great Insect Fair, the Plant Sciences Educational & Enrichment Academy, and the Food and Agricultural Sciences and Industries Minority Recruitment Program, designed to expose minority high school students to careers in the agricultural sciences and to research possibilities in entomology.

Progress 07/01/12 to 06/30/16

Outputs
Target Audience:Farmers, agricultural researchers, plant scientists, extension staff, other agricultural professionals, entomologists, US Forest Service researchers and specialists, Integrated Pest Management specialists, Biological Control specialists, home owners, land owners, municipalities. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Undergraduate and graduate students and postdoctoral researchers are involved in this research, providing valuable training and first-hand research experience for least fifteen scientists across all participating labs. How have the results been disseminated to communities of interest?We have published our results in peer-reviewed journals, national and international scientific meetings, including presentations in China, Italy, Brazil, Sweden, and Bangladesh. We also shared appropriate portions of our research at extension meeting through out Pennsylvania. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? We studied various aspects of the chemical ecology of species interactions, ranging from traditional plant-insect interactions to mushroom-insect interactions, plants ability to sense herbivores, and intra-hive communications in honey bees. Importantly, we are studying organism, their behavior, as well as sub-organismal details. On the organismal side, we continue to explore our line of inquiry that revealed that plants are capable of detecting volatile cues associated with their herbivores. We continue to study this system of tall goldenrod (Solidago altissima) which can alter its physiology in response to the putative sex pheromone of its specialist herbivore, Eurosta solidaginis. We also found that decreases in herbivory associated with exposure to the pheromone are indeed associated with changes in plant physiology, and are not related to some deterrent capacity of the male pheromone itself. More recent work is focusing on the distance over which this pheromone exposure operates and the duration of the effect. Our field work has revealed that nearby plants (within 10 cm) can also sense the pheromone, induce their defenses, and receive less damage following pheromone exposure and that this effect plant defenses lasts for about one week. Because nearby plants also benefit from detecting and responding to the fly pheromone, we know that the community of insects on these plants changes. Therefore, in fields of S. altissima with good populations of E. solidaginis, it appears that during the active period of adult flies they induce a mosaic of primed and unprimed plants and that respond differently when attacked by insect herbivores, creating a patchwork of more or less acceptable host plants, which in turn support different communities of insect species. We have also begun working with bumble bees to understand whether nutrition preferences drive their forage behavior. Our work indicates that it does, and that the protein to lipid ratio of pollen explains much of the pattern of bumble bee foraging. We continue to work on associations among phytohormones, plant defenses, and gall insects and have developed a phytohormones-based hypothesis for the evolution of the gall-inducing habit in insects. We have identified a small set of fungal species present during mushroom cultivation that are attractive to female sciarid mushroom flies, i.e., the fungus gnat species, Lycoriella ingenua. Some of these were found on the bodies of gravid females and may explain how infestations get started in mushroom houses. Other fungal species having different degrees of attractiveness to females are those commonly found in mushroom compost. We found that some fungal species that were not attractive to females are very strong oviposition stimulants to females, and so we hypothesize that the volatiles from some fungi attract the females to parts of the compost, and other fungi then stimulate the females to lay their eggs there. We found that larvae can develop to adulthood by feeding on the mycelia of only three different fungal species, and for all the other species, the larvae die before making it past the first larval stage. We have also isolated an active female-emitted sciarid mushroom fly sex pheromone component, a sesquiterpene alcohol that is a type of germacradienol, that is highly active in attracting males. This work proves that a compound identified as a sex pheromone in 1980 by a different research group was an erroneous and misleading identification that has hampered research into finding a true and highly active sex pheromone such as the one we have isolated. We are currently attempting to characterize the precise stereochemical structure of this very difficult and first-ever discovered form of germacradienol, and have formed collaborative research efforts with top-notch sesquiterpene chemists from Germany, England, the U. S., and Costa Rica. We made significant progress in finding ways to improve attractants for the Asian longhorned beetle (ALB; Anoplophora glabripennis). In order to try to improve this now commercially available lure we have continued to perform single cell recordings from antennal olfactory sensory neurons (OSNs), have now obtained confocal microscope images of male and female antennal lobe glomeruli that have determined how many glomeruli they contain, and have begun to correlate these glomeruli to sex pheromone and plant volatile olfaction in the two sexes. We have reconstructed confocal microscope images of the antennal lobes into the first-ever 3D Atlases for this species, for which a number of different glomeruli have been assigned names for relating their architecture and topographical location to those of other species. In work on a new invasive species, Lycorma deliculata, the spotted lanternfly (SLF; Hemiptera: Fulgoridae), we collected samples of honeydew emitted by feeding insects, which we observed to be in large all-female aggregations. We were unable to begin screening the compounds in these samples for behavioral attraction. It became apparent that the insects are not yet amenable to colony rearing, as they usually died within a week of being placed in captivity. This inability to rear these fulgorid bugs has delayed the work related to other goals such as conducting GC-EAD analysis of volatiles, and testing various odorants for attraction. In the meantime, a detailed phenological observational study of adult males and females was performed to enlighten us about the potential ecological context for any insect semiochemical attraction. A manuscript is being prepared that summarizes this work. We began collecting volatiles from males, females, and male-female combinations on ailanthus tree leaves in the field. We have also studied the malaria vector Anopheles gambiae, which is attracted to the American weed, Parthenium hysterophorus that is invasive in large areas of Africa. The mosquito feeds on nectar from the plant and our preliminary evidence suggests that chemicals from the plant enhance the malaria parasite in the mosquito.

Publications

  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Nyasembe, V., Teal, P.E.A., Sawn, P., Tumlinson, J.H., Borgemeister, C., and Torto, B. Plasmodium falciparum infection increases Anopheles gambiae attraction to nectar sources and sugar uptake. Current Biology 24: 217-221 (2014).
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Ray, S., I. Gaffor, F. Acevedo, A. M. Helms, W.-P. Chuang, J.F. Tooker, G. W. Felton, D. S. Luthe. 2015. Maize plants recognize herbivore-associated cues from caterpillar frass. Journal of Chemical Ecology 41: 781792
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Richter, A., Seidl-Adams, I., Ko�llner, T.G., Schaff, C., Tumlinson, J.H., Degenhardt, J. A small, differentially regulated family of farnesyl diphosphate synthases in maize (Zea mays) provides farnesyl diphosphate for the biosynthesis of herbivore-induced sesquiterpenes. Planta 241:13511361 (2015).
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Vaudo, A. D., H. M. Patch, D. A. Mortensen, C. M. Grozinger, and J. F. Tooker. 2014. Bumble bees exhibit daily behavioral patterns in pollen foraging. Arthropod-Plant Interactions 8: 273-283.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Vaudo, A. D., H. M. Patch, D. A. Mortensen, J. F. Tooker, C. M. Grozinger. 2016. Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences. Proceedings of National Academy of Science USA 113:E4035-42.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Vaudo, A. D., J. F. Tooker, C. M. Grozinger, and H. M. Patch. 2015. Bee nutrition and floral resource restoration. Current Opinion in Insect Science 10: 133141.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Walls, J. T, P. Caciagli, J. F. Tooker, J. M. Russo, E. G. Rajotte, C. Rosa. 2016. Modeling the decision process for barley yellow dwarf management. Computers and Electronics in Agriculture 127: 775786.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Yoshinaga, N., Abe, H., Morita, S., Yoshida, T., Aboshi, T., Fukui, M., Tumlinson, J.H., and Mori, N. Plant volatile eliciting FACs in lepidopteran caterpillars, fruit flies, and crickets: a convergent evolution or phylogenetic inheritance? Frontiers in Physiology, 5: 5: 121-127 (2014).
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Bohnenblust, E. W., A. D. Vaudo, J. F. Egan, D. A. Mortensen, and J. F. Tooker. 2016. Effects of the herbicide dicamba on non-target plants and pollinator visitation. Environmental Toxicology and Chemistry 35: 144151.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Grettenberger, I. M. and J. F. Tooker. 2016. Inter-varietal interactions among plants in genotypically diverse mixtures tend to decrease herbivore performance Oecologia 182: 189-202.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Nyasembe VO, Cheseto X, Kaplan F, Foster WA, Teal PEA, Tumlinson JH, et al. (2015) The Invasive American Weed Parthenium hysterophorus Can Negatively Impact Malaria Control in Africa. PLoS ONE 10(9): e0137836. doi:10.1371/ journal.pone.0137836


Progress 10/01/14 to 09/30/15

Outputs
Target Audience:Agricultural researchers, plant scientists,extension staff, other agricultural professionals, and entomologists. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Undergraduate and graduate students and postdoctoral researchers are involved in this research, providing valuable training and first-hand research experience for least fifteen scientists across all three participating labs. How have the results been disseminated to communities of interest?We have published our results in peer-reviewed journals, national and international scientific meetings, including presentations in China, Italy, and Bangladesh. We also shared appropriate portions of our research at extension meeting through out Pennsylvania. What do you plan to do during the next reporting period to accomplish the goals?We will continue to pursue current research leads. We will finish characterizing details of the ability of goldenrod to detect its specialist herbivore, the distance over which the pheromone is active, the dose the plant needs to receive, and how long the effect lasts. We are also exploring the evolutionary trade-off for the fly whose pheromone tips off the plant to its presence, potentially influencing the success of its offspring. During the coming year, we plan to continue to explore the role of insect- and plant-derived elicitors in triggering host plant defenses. We will also use our knowledge of Asian long-horned beetle olfaction to develop a more efficient sex pheromone trap for this pest species. We plan to try to finalize the identification of the sex pheromone of the mushroom fly, L. ingenua, and if this is accomplished, and if we can obtain synthetic samples of the sex pheromone, we will start field trapping experiments using this pheromone, in and around mushroom houses. From our work with host-plant volatiles of ash trees, data will be analyzed in an effort to determine whether specific VOC cues emitted by trunks of as trees and white fringe trees guide EAB females to suitable hosts. Further data will be collected during the summer of 2016 if requested funding is received. Research is continuing on the role of VOC in plant defense against herbivory and inplant-plant communication.

Impacts
What was accomplished under these goals? We continue to study various aspects of the chemical ecology of species interactions, ranging from traditional plant-insect interactions to mushroom-insect interactions, plants ability to sense herbivores, and intra-hive communications in honey bees. Importantly, we are studying organism, their behavior, as well as sub-organismal details. On the organismal side, we continue to explore our line of inquiry that revealed that plants are capable of detecting volatile cues associated with their herbivores. We continue to study this system of tall goldenrod (Solidago altissima) which can perceive and responds alter its physiology in response to the putative sex pheromone of its specialist herbivore, Eurosta solidaginis. We also found that decreases in herbivory associated with exposure to the pheromone are indeed associated with changes in plant physiology, and are not related to some deterrent capacity of the male pheromone itself. Recent work is determining the distance over which this pheromone exposure operates and the duration of the effect. On the sub-organismal side, we are investigating the biochemical mechanisms by which fatty acid-amino acid conjugates, trigger plant chemical defenses. We are also investigating the mechanisms by which plants perceive and respond to volatile organic compounds from neighboring damaged plants. Emphasis is on developing fundamental knowledge and principles that can be applied in environmentally safe pest management programs. Recently, we also performed the first-ever single-sensillum recordings on the Asian long-horned beetle and shown that the olfactory system does have neurons tuned to this species' two sex pheromone components. We also isolated and tentatively identified the major sex pheromone component of the mushroom fly pest species, Lycoriella ingenua. We developed a novel, non-sticky trap for the emerald ash borer that utilizes 3D-printed artificial female beetle decoys. We also studied the flow of synthetic plant secondary metabolites (i.e., systemic neonicotinoid insecticides) through an invertebrate food web, and studied the non-target effects of these ubiquitous agricultural compounds.We also analyzed by GC and GC-MS volatile organic compounds (VOC) collected from trunks of ash and white fringe trees in Ohio. The Cipollini lab, Wright State University collected emerald ash borer oviposition data from the same trees at the same time. Data are now being analyzed to correlate VOC and oviposition data to determine if VOC cues guide different levels of EAB oviposition on different species of trees. In collaboration with Prof S. Kang, PSU, we analyzed VOC produced by various fungal species to determine if fungal VOC are affecting Arabidopsis growth. There was not correlation of fungal VOC with plant growth. However, measurment of fungal produced carbon dioxide strongly indicated that fungal CO2 was the primary factor affecting plant growth. We also found that emission of green leaf volatiles (GLV) by corn seedlings at the onset of darkness is greater in herbivore elicitor treated corn seedlings than in controls.

Publications

  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Grettenberger, I. M., and J. F. Tooker. 2015. Moving beyond resistance management toward an expanded role for seed mixtures in agriculture. Agriculture, Ecosystems and Environment 208:2936. DOI:10.1016/j.agee.2015.04.019
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Douglas, M. R., and J. F. Tooker. 2015. Large-Scale Deployment of Seed Treatments Has Driven Rapid Increase in Use of Neonicotinoid Insecticides and Preemptive Pest Management in U.S. Field Crops. Environ. Sci. Technol. 49(8): 0885097
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Douglas, M. R., J. R. Rohr, and J. F. Tooker. 2015. Neonicotinoid insecticide travels through a soil food chain, disrupting biological control of non-target pests and decreasing soybean yield. Journal of Applied Ecology 52:250260. (Editors Choice article and image from the article featured on the cover, DOI: 10.1111/1365-2664.12372; and read our Research Brief on the topic, and a related post in the blog of the Journal of Applied Ecology.)
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Meng, P. S., Trotter, R. T., Keena, M. A., Baker, T. C., Yan, S., Schwartzberg, E. G. and Hoover, K. (2014) Effects of pheromone and plant volatile release rates and ratios on trapping Anoplophora glabripennis (Coleoptera: Cerambycidae) in China. Environ. Entomol. 43: 379-1388.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Domingue, M. J., Lakhtakia, A., Pulsifer, D. P., Hall, L. P., Badding, J. V., Bischof, J. L., Martin-Palma, R. J., Imrei, Z., Janik, G., Mastro, V. C., Hazen, M., and Baker, T. C. (2014) Bioreplicated visual features of nanofabricated buprestid beetle decoys evoke stereotypical male mating flights. Proc. Nat. Acad. Sci. (USA) DOI/10.1073/pnas.1412810111.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: George, J., Blanford, S., Thomas, M. B., and Baker, T. C. (2014) Malaria mosquitoes host-locate and feed upon caterpillars. PLoS ONE 9: e108894 doi:10.1371/journal.pone.0108894
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: T�th, M., Viana, P.A., Vilela, E., Domingue, M. J., Baker, T. C., and Vuts, J. (2014) KLP+ (hat) trap with semiochemical lures suitable for trapping two Diabrotica spp. exotic to Europe. Acta Phytopath. Entomol. Hungarica 49:211-221.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Villar, G. Baker, T. C., Patch, H. M., and Grozinger C. M. (2015) Neurophysiological mechanisms underlying sex-and maturation-related variation in pheromone responses in honey bees (Apis mellifera). J. Comp. Physiol. A 201:731-739.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Yoshinaga, N., Ishikawa, C., Seidl-Adams, I., Bosak, E., Aboshi, T., Tumlinson, J.H., and Mori, N. N-(18-Hydroxylinolenyl)-L-Glutamine: A newly discovered analog of volicitin in Manduca sexta and its elicitor activity in plants. J. Chem. Ecol. 40:484-490 (2014).
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Domingue, M. J., Pulsifer, D. P., Lakhtakia, A., Berkebile, J., Steiner, K. C., Lelito, J. P., Hall, L. P., and Baker, T. C. (2015) Detecting emerald ash borers (Agrilus planipennis) using branch traps baited with 3D-printed beetle decoys. J. Pest. Sci. 88:267-279.


Progress 10/01/13 to 09/30/14

Outputs
Target Audience: Ecologists, entomologists, and evolutionary biologists. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Several graduate and undergraduate students, and at least one high school student, received training during our research efforts. From June 1st to June 15th 2o14, we also organized and presented Penn State’s Center for Chemical Ecology international short course in insect chemical ecology entitled “ICE14”. This is the highly successful course that rotates yearly between the Swedish Agricultural University at Alnarp, the Max Planck Institute for Chemical Ecology, and Penn State University. Penn State last hosted the course in 2010. The enrollment for ICE 14 was 42 students from 14 countries, surpassing the enrollment for ICE 10 here at Penn State of 29 students. The students came from Brazil (3), Botzwana (1), China (2), Nigeria (2), Kenya (3), Sweden (1), Belgium (2), Italy (1), France (1), Germany (2), India (1), French Guiana (1), Japan (2), Canada (4) and the U.S. (18). Students from the U.S. other than from Pennsylvania came from California, Montana, New Jersey, Arkansas, Indiana, and Florida. Also included was one senior scientist from the USDA/ARS. There were 22 different guest lecturers, all of whom are recognized international experts in their sub-discipline within chemical ecology. Among these lecturers were 11 guest speakers from France, Germany, England, Sweden, Nigeria, and Australia. Other guest speakers from the U.S. came from U.C. Riverside and Cornell University. Students were exposed to subject matter in the following areas: 1) sensory biology and evolution; 2) insects and pathogens; 3) applied uses of pheromones and other semiochemicals; 4) semiochemical discovery, isolation, identification and synthesis; 5) plant-insect interactions; 6) pollination ecology; 7) and the evolution of odor-mediated behavior. All of the students were required to present a poster on their research during an evening poster session on the first day of the course, plus a five-minute lecture on their research during the day. They were treated to a field trip to the Penn State Tree Fruit Research and Extension Center in Biglerville, where they heard a lecture about the use of pheromones in tree fruit Integrated Pest Management and then toured a commercial orchard nearby where the owner showed the students the various mating disruption dispensers that he uses on his apples and peaches to control various moth pests. Students were appreciative of the efforts of the host-organizers of the course, Jim Tumlinson and Tom Baker, who were presented with honorary ICE 14 T-shirts designed and purchased by the students to mark their participation in the course that they were all so excited to have been a part of. Written comments from one student from ICIPE in Kenya after the course epitomizes the sentiments of so many of the other students. He wrote, “I remember the Penn State experience: the whole of it. For me it was the defining moment of my understanding and love for the field of chemical ecology. I can remember almost every lecture and my colleagues are a little tired of me telling it to them over and over. I received late last week two envelopes: one with a memory stick with all lectures and another with my participation certificate. You will never know how grateful I am for you having considered me for the opportunity and for your kindness throughout. As for my friends, it's only just begun. Now I have slides to start re-telling the stories again! Now I am working my PhD with renewed spirit, correcting mistakes I had already made not being in the know of the vast world of chemical ecology. If all goes well I should finish by the end of this year. How have the results been disseminated to communities of interest? Presentations at national and international research meetings, seminars in entomology departments around the country, Penn State outreach events, and through ICE14. What do you plan to do during the next reporting period to accomplish the goals? We will continue to pursue the objectives to reveal to influence of chemical ecology in basic and applied research systems.

Impacts
What was accomplished under these goals? More effective and sustainable approaches to managing and controlling herbivorous insect pests will be developed based on knowledge of the fundamental mechanisms of insect herbivores intereactions with their host plants, including the mechanisms by which plants defend against insect herbivory and the role of herbivore-produced elicitors of plant defenses in the insects’ metabolism. Further, some pest management tactics rely on doses of pheromones of herbivores either to traps individuals (pheromone trapping) or to confuse potential mates (i.e., mating disruption); our results suggest that pheromone use may trigger host plant defenses, potentially with fitness costs to the focal plant species.

Publications

  • Type: Journal Articles Status: Awaiting Publication Year Published: 2014 Citation: Seidl-Adams, I., Richter, A., Boomer, KB, Yoshinaga, N., Degenhardt, J., and Tumlinson, J. H. Emission of herbivore elicitor-induced sesquiterpenes is regulated by stomatal aperture in maize (Zea mays) seedlings). Plant Cell and Environ. (In Press). (2014).
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Tumlinson, J.H. The Importance of Volatile Organic Compounds in Ecosystem Functioning. J. Chem. Ecol. 40:212-213 (2014).
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Elliud Muli,, Harland Patch, Maryann Frazier, James Frazier, Baldwyn Torto, Tracey Baumgarten, Joseph Kilonzo, James Nganga Kimani, Fiona Mumoki, Daniel Masiga, James Tumlinson, Christina Grozinger. Evaluation of the Distribution and Impacts of Parasites, Pathogens, and Pesticides on Honey Bee (Apis mellifera) Populations in East Africa. PLOS one, 9(4):e94459 (2014).
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Yoshinaga, N., Ishikawa, C., Seidl-Adams, I., Bosak, E., Aboshi, T., Tumlinson, J.H., and Mori, N. N-(18-Hydroxylinolenyl)-L-Glutamine: A newly discovered analog of volicitin in Manduca sexta and its elicitor activity in plants. J. Chem. Ecol. 40:484-490 (2014).
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Tooker, J. F., and A. M. Helms. 2014. Phytohormone dynamics associated with gall insects, and their potential role in the evolution of the gall-inducing habit. Journal of Chemical Ecology 40:742-753.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Helms, A. M., C. M. De Moraes, M. C. Mescher, and J. F. Tooker. 2014. The volatile emission of Eurosta solidaginis primes herbivore-induced volatile production in Solidago altissima and does not directly deter insect feeding. BMC Plant Biology 14:173.
  • Type: Journal Articles Status: Awaiting Publication Year Published: 2014 Citation: Yoshinaga, N., Abe, H., Morita, S., Yoshida, T., Aboshi, T., Fukui, M., Tumlinson, J.H., and Mori, N. Plant volatile eliciting FACs in lepidopteran caterpillars, fruit flies, and crickets: a convergent evolution or phylogenetic inheritance? Frontiers in Physiology, 5: (In Press). (2014).
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Toth, A. L., J. F. Tooker, S. Radhakrishnan, R. Minard, M. T. Henshaw, C. M. Grozinger. Shared genes related to aggression, rather than chemical communication, are associated with reproductive dominance in paper wasps (Polistes metricus). BMC Genomics 15(1):75.


Progress 10/01/12 to 09/30/13

Outputs
Target Audience: Ecologists, chemical ecologists, entomologists, plant biologists, pest managers, extension faculty, extension educators, master gardeners. USDA/APHIS plant protection and quarantine specialists; U. S. Forest Service researchers and specialists; Integrated Pest Management specialists; Biological Control specialists; home owners, land owners, and municipalities in areas where the emerald ash borer is threatening destruction of ash trees; foresters and forest owners in the Northeastern U.S.; For the insect-antenna-based chemosensor, researchers interested in improved chemosensing technologies for homeland and agricultural security and food safety. For our malaria mosquito work, researchers around the world interested in reducing malaria transmission through altering mosquito behavior. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? All of our projects involved graduate students and/or postdoctoral scientists, so each project offers training opportunities for these early career scientists. The students and postdoc also have the opportunity to mentor undergraduate assistants (grad students and postdocs) and graduate students (postdoc) as their project progress, providing an opportunity to direct a team and make efficient use of staff time. How have the results been disseminated to communities of interest? Publications (journal papers, book chapters), invited seminars and talks, submitted presentations at national and regional scientific meetings. What do you plan to do during the next reporting period to accomplish the goals? We will continue following the research paths we have started to further elucidate the phenomena and mechanisms we have discovered.

Impacts
What was accomplished under these goals? Both female Lygus bugs and their natural enemies, female P. relictus wasps, are highly attracted to Erigeron. annuus volatiles over those of cotton in almost every combination of damage treatments. Results suggest that E. annuus would be an effective trap plant to control Lygus in cotton, since it is highly attractive to both the pest and its natural enemy. We discovered that tall goldenrod (Solidago altissima), a common old-field plant species in the eastern United States, can perceive andrespond to the volatile emission (putative sex pheromone) of its specialist herbivore, the tephritid fly Eurosta solidaginis. After being exposed to the fly-derived volatile compound, the plant defenses are primed, and upon herbivory, male-exposed plants have an enhanced, jasmonic-acid-mediated defensive response compared to unexposed plants. Further, female E. solidaginis are deterred from male-exposed plants. We found that genotypically diverse cultivar mixtures of wheat release more complex bouquets of plant volatiles, which may repeal aphid species and possibly attract natural enemies. Our work during this project-reporting period has provided new progress toward developing an effective detection tool for invasive buprestid beetle species through understanding the mate-finding and mate-acceptance behaviors of buprestid beetles in the field. We now have investigated newly invasive species in their home forests in central Europe, and found that these species also use a similar system to those we have investigated in N. America, in which patrolling males visually locate and aerially pounce on females that are resting in sunlight on host tree foliage. The use of dead female or male models of these species that are pinned to host tree leaves in the field causes feral males of these species to dive onto and land upon the models. This is the behavior we are developing for use in highly sensitive traps. Our work on an insect antenna-inspired chemosensor has resulted in a novel gas-chromatographi/electroantennogram detection system (GC/EAD) that has several orders of magnitude greater sensitivity and resolution ability in detecting compounds eluting from the GC. We broke new ground in mosquito olfaction-mediated behavior, showing that Anopheles stephensi females that were infected with the fungus, Beauveria bassiana, exhibited impaired olfactory receptor neuron responsiveness to the vertebrate host volatile, 1-octen-3-ol. This reduction in olfactory acuity corresponds to a reduced behavioral responsiveness to vertebrate host volatiles. We also determined that the malaria mosquito, Anopheles stephensi, when infected with the malaria parasite Plasmodium yoelii, exhibits both decreases and increases in mammalian host-seeking behavior that are correlated with corresponding changes in the sensitivity of olfactory receptor neurons on the mosquito’s maxillary palps.

Publications

  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Pulsifer, D. P., Lakhtakia, A., Narkhede, M. S., Domingue, M. J., Post, B. G., Kumar, J., Mart�n-Palma, R. J., and Baker, T. C. (2013) Fabrication of polymeric visual decoys for the male emerald ash borer (Agrilus planipennis). J. Bionic Eng. 10: 129-138. DOI: 10.1016/S1672-6529(13)60207-3.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: George, J., Jenkins, N. E., Blanford, S. Thomas, M. B., and T. C. Baker. (2013) Malaria mosquitoes attracted by fatal fungus. PLOS ONE. 8: Issue: 5 Article Number: e62632 DOI:10.1371/journal.pone.0062632.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Cator, L. J., George, J. Blanford, S. Murdock, C. C., Baker, T.C., Read, A. F., and M. B. Thomas (2013). Manipulation without the parasite: altered feeding behavior of mosquitoes is not dependent on infection with malaria parasites. Proc. Roy. Soc. B 280: 20130711. http://dx.doi.org/10.1098/rspb.2013.0711.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Domingue, M. J., Imrei, Z., Lelito, J., Muskovits, J., Janik, J., Cs�ka, G., Mastro, V., and T. C. Baker. (2013) Trapping of European buprestid beetles in oak forests using visual and olfactory cues. Entomol. Exp. Appl. 148: 116-129. DOI: 10.1111/eea.12083.
  • Type: Book Chapters Status: Published Year Published: 2012 Citation: Domingue, M. J., and Baker, T. C. (2012) A multi-disciplinary approach for developing tools to monitor invasive buprestid beetle species. In: Invasive Species, J. J. Blanco and A. T. Fernandes (eds). Nova Science Publishers, Inc. pp. 77-100. ISBN: 978-1-61942-761-7.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Halloran, S.T., Mauck, K.E., Fleisher, S.F. and Tumlinson, J.H. Volatiles from Intact and Lygus-Damaged Erigeron annuus (L.) Pers. are Highly Attractive to Ovipositing Lygus and its Parasitoid Peristenus relictus Ruthe. J Chem Ecol. 39:11151128 (2013).
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Helms, A. M., C. M. De Moraes, J. F. Tooker, and M. C. Mescher. 2013. Exposure of Solidago altissima plants to volatile emissions of an insect antagonist (Eurosta solidaginis) deters subsequent herbivory. Proceedings of National Academy of Science USA 110:199-204.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Shoffner, A. V., and J. F. Tooker. 2013. The potential of genotypically diverse cultivar mixtures to moderate aphid populations in wheat (Triticum aestivum L.). Arthropod-Plant Interactions 7:33-43.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Tian, D., Tooker, J. F., Peiffer, M., Chung, S., and G. W. Felton. 2012. Role of Trichomes in Defense against Herbivores: Comparison of Herbivore Response to Woolly and Hairless Trichome Mutants in Tomato (Solanum lycopersicum). Planta 236:1053-66.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Kim J, J. F. Tooker, D. S. Luthe, C. M. De Moraes, and G. W. Felton. 2012. Insect egg can enhance wound response in plants: a study system of tomato Solanum lycopersicum L. and Helicoverpa zea Boddie. PLoS ONE 7(5):e37420. doi:10.1371/journal.pone.0037420
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Tian, D, M. Peiffer, E. Shoemaker, J. Tooker, E. Haubruge, E. Francis, D. S. Luthe, and G. W. Felton. Salivary glucose oxidase from caterpillars mediates the induction of rapid and delayed-induced defenses in the tomato plant PLoS ONE 7(4):e36168. doi:10.1371/journal.pone.0036168
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Frost, C. J., E. C. Smyers, J. M. Dean, M. C. Mescher, J. E. Carlson, C. M. De Moraes, and J. F. Tooker. A petiole-galling insect herbivore decelerates leaf lamina litter decomposition rates. Functional Ecology 26:628636. DOI:10.1111/j.1365-2435.2012.01986.x
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Tooker, J. F. and S. D. Frank. 2012. Genotypically diverse cultivar mixtures for insect pest management and increased crop yields. Journal of Applied Ecology 49:974-985.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Kariyat RR, Mauck KE, Balogh CM, Stephenson AG, Mescher MC, & De Moraes CM. 2013. Inbreeding in horsenettle (Solanum carolinense) alters night-time volatile emissions that guide oviposition by Manduca sexta moths. Proceedings of the Royal Society B 20130020.http://dx.doi.org/10.1098/rspb.2013.0020
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Salvaudon L, De Moraes CM & Mescher MC. 2013. Outcomes of co-infection by two potyviruses: implications for the evolution of manipulative strategies. Proceedings of the Royal Society B B 20122959. http://dx.doi.org/10.1098/rspb.2012.2959
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Kariyat, RR, Balogh, CM, Moraski, RP, De Moraes, CM, Mescher, MC, & Stephenson, AG. 2013. Constitutive and herbivore-induced structural defenses are compromised by inbreeding inSolanum carolinense L. American Journal of Botany, doi:10.3732/ajb.1200612
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Salvaudon, L, CM De Moraes, JY Yang, NH Chua & MC Mescher.2013. Effects of the virus satellite gene ?C1 on host plant defense signaling and volatile emission. Plant Signaling & Behavior 8 (3), e23317
  • Type: Book Chapters Status: Published Year Published: 2013 Citation: Rodriguez-Saona, CR. CM De Moraes,& MC Mescher. 2013. The Role of Volatiles in PlantPlant Interactions. F. Baluaka (ed.), Long-Distance Systemic Signaling and Communication in Plants,Signaling and Communication in Plants 19, DOI10.1007/978-3-642-36470-9_19, Springer-Verlag Berlin Heidelberg.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Smith JD, Mescher MC, & De Moraes CM. 2013. Bottom-up effects of bioactive solute transfer from hosts to parasitic plants. Current Opinion in Plant Biology 16:464-472. http://dx.doi.org/10.1016/j.pbi.2013.06.016
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Verheggen, F.J., E. Haubruge, C.M. De Moraes and M.C. Mescher. 2009. Aphid responses to volatile cues from turnip plants (Brassica rapa) infested with phloem-feeding and chewing herbivores.Arthropod-Plant Interactions http://dx.doi.org/10.1007/s11829-013-9272-1.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Baker, T. C., Domingue, M. J., and Myrick, A. J. (2012) Working range of stimulus flux transduction determines dendrite size and relative number of pheromone component receptor neurons in moths. Chemical Senses 37:299-313 doi: 10.1093/chemse/bjr122.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Myrick, A. J., and Baker, T. C. (2012) Chopper-Modulated Locked in Amplified Gas Chromatography - Electroantennography Part II: Signal Processing and Performance Comparisons. IEEE Sensors Journal 12:2974-2983.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Pulsifer, D. P., Lakhtakia, A., Kumar, J., Baker, T. C., and Martin-Palma, R. J. (2013) Toward pest control via mass production of realistic decoys of insects. Proc. SPIE Vol 8686: UNSP 86860L. doi:10.1117/12.2010021.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Domingue, M. J., Lelito, J. P., Fraser, I., Mastro, V. C., Tumlinson, J. H., and Baker, T. C. (2013). Visual and chemical cues affecting the detection rate of the emerald ash borer in sticky traps. J. Appl. Entomol. 137:77-87. DOI:10.1111/j.1439-0418.2012.01737.x


Progress 10/01/11 to 09/30/12

Outputs
OUTPUTS: Work from this project seeks to enhance understanding of plant-plant and plant-insect interactions, plant community interactions, and disease ecology. This project generated publications in high impact journals, presentations at meetings and outreach to the community. We documented characteristic olfactory cues associated with the infection of squash plants by powdery mildew, including the emission of characteristic compounds that have previously been reported from other fungi and elevated emissions of apparently plant-derived compounds that may be induced by fungal infection. We are also investigating inbreeding depression in horsenettle (Solanum carolinense) to understand how inbred plants suffer more herbivory than outbred plants. These results are providing valuable insight on the cost of inbreeding depression for plants. We have also demonstrated that volatile organic compounds from host trees are attractive to the invasive wood wasp, Sirex noctilio and identified a male-produced pheromone for this species. A blend of voc attractive to the malaria vector, Anopheles gambiae, and based on plant produced was also identified. We also explored factors influencing herbivore distributions in plant communities. Different crop cultivars possess variable resistance to their herbivores, including aphids. When crop varieties are mixed together to form cultivar mixtures of single species, the resistance of the plant community increases and the aphid populations that mixtures support is significantly less than those supported by monocultures of mixtures. Volatile cues to foraging aphids are also quite distinct between mixtures and monocultures, providing a mechanism for aphids to discriminate between treatments. PARTICIPANTS: Nothing significant to report during this reporting period. TARGET AUDIENCES: Nothing significant to report during this reporting period. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
Further development of basic knowledge of the interactions of insect herbivores and their host plants, including the mechanisms by which plants defend against insect herbivory and the role of herbivore-produced elicitors of plant defenses in the insects' metabolism, will enhance our ability to develop more effective methods of biological control of insect pest of agricultural crops. Our work is improving our basic understanding of the mechanisms of plant defenses against insect pests, providing more information of potential use for designing pest management strategies. Identification of chemical signals that affect mating in invasive species or disease vectors may increase effectiveness of detection, monitoring, and management of these pests.

Publications

  • No publications reported this period