Source: UNIVERSITY OF FLORIDA submitted to NRP
INTEGRATED MANAGEMENT OF KEY INSECT PESTS AFFECTING FLORIDA CITRUS PRODUCTION
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
0213142
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Oct 1, 2007
Project End Date
Sep 30, 2013
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
UNIVERSITY OF FLORIDA
G022 MCCARTY HALL
GAINESVILLE,FL 32611
Performing Department
Citrus Research and Education Center
Non Technical Summary
Several insect pests affect Florida citrus production through direct feeding damage and/or spread of disease. The Asian citrus psyllid, Diaphorina citri, is a vector of citrus greening disease, while citrus leafminer, Phyllocnistis citrella, and Diaprepes root weevil, Diaprepes abbreviatus, infestations facilitate tree infection by canker and Phytophthora, respectively. This project intends to develop effective and biorational monitoring and control strategies for each of these pests. This will be achieved by identifying attractive semiochemicals as well as developing eco-friendly pest management solutions such as mating disruption and Bacillus thuringiensis (Bt) toxin formulations. In addition, research will be conducted on compatibility of current and future pest management tactics with the effectiveness of natural enemies.
Animal Health Component
(N/A)
Research Effort Categories
Basic
(N/A)
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2110999107060%
2160999113040%
Goals / Objectives
Objectives: 1) To develop reliable monitoring technologies and protocols for current major pests of Florida citrus including Asian citrus psyllid (ACP), Diaphorina citri, citrus leafminer (CLM), Phyllocnistis citrella, and Diaprepes root weevil (DRW), Diaprepes abbreviatus; 2) To develop pheromone-based mating disruption for CLM control as an alternative or supplement to insecticides; 3) To evaluate experimental insecticide formulations for control of key citrus pests and develop effective application protocols leading to their registration and commercial use; 4) To improve DRW control by entomopathogenic nematodes and Bacillus thuringiensis toxins; 5) To investigate insect-mediated mechanisms of disease transmission in citrus and develop methods for mitigating disease spread; 6) To determine impact of current pest control practices on populations of natural enemies and develop cultural practices for conservation of biological control agents.
Project Methods
Development of effective monitoring programs will allow for more precise forecasting of the need for insecticide applications and will reduce chemical inputs in citrus through judicious, need-based application. Trap design and deployment protocols will be optimized for monitoring of CLM males and a catch-based treatment threshold will be developed for insecticide sprays targeting CLM. Determining the role of sex pheromones and plant chemicals in ACP and DRW biology may lead to identification of attractants. The dispersal behavior of ACP will be investigated as well as the physiological basis of disease transmission. This basic information will be used to develop tactics for mitigating disease spread within and among groves. The effect of current management practices on natural enemy populations and parasitization rates will be determined. Control tactics will be appropriately modified or developed to promote efficacy of natural enemies.

Progress 10/01/07 to 09/30/13

Outputs
Target Audience: 1) Citrus industry clientele in Florida and worldwide. 2) Commenrcial fruit, vegatable and agroforestry growers. 3) Fruit growing industry personel, with particular focus on citrus. 4) International students and interns interested in plant-insect interactions, chemical ecology, insect behavior, and pest management. 5) Entomology and Nematology, Phytopathology, and Plant Biology students at University of Florida and other U.S. institutions. Changes/Problems: While certain exotic pests and pathogens, such as citrus root weevil species (example: Diaprepes abbreviatus (L.)), citrus leafminer, Pyllocnistis cytrella Stainton, and citrus bacterial canker, Xanthomonas axonopodis (Hasse), have proven challenging to manage in Florida citrus and required unusual efforts of chemical input or tree removal as compared with most other pests and diseases in citrus, the arrival of the Asian citrus psyllid, Diaphorina citri Kuwayama, in Florida in the 1990s and the associated identification of a tree-killing disease, Huanglongbing (HLB), in Florida in 2005 (Grafton-Cardwell et al. 2013) essentially eliminated several decades of effort to develop effective IPM practices in Florida citrus. The disease is caused by a bacterial pathogen that this psyllid vector transmits. The pathosystem transformed Florida citriculture due to the severity of this disease with respect to tree decline and possible tree death. The associated need for intensive vector management to maintain existence of productive trees has resulted in a near elimination of previously effective biological control in Florida citrus (Grafton-Cardwell et al. 2013). Citrus growers in Florida are finding it increasingly difficult to maintain low HLB incidence in their plantings and to remain profitable, even as they implement inoculum removal via infected tree removal, multiple insecticide application strategies believed to be effective in keeping disease rates low, and enhanced nutritional programs which aim to reduce the impact of disease symptoms. The importance of effective vector control has risen as many growers are abandoning the strategy of inoculum removal and instead attempting to prolong life and productivity of diseased trees with intense supplemental applications of micronutrients. These strategies are costly; moreover, with eroding success in controlling HLB incidence possibly due to high surrounding inoculum pressure, it is becoming increasingly difficult to accomplish effective control. The loss of an insecticide due to development of resistance may be a future further blow to an industry that relies on insecticides for D. citri control and management of other significant pests. Long-term HLB solutions such as resistant citrus cultivars and other methods of blocking HLB transmission by the vector may succeed in the future, but they will take time, perhaps decades, to develop. D. citri quickly became established throughout the state, making its eradication impossible. Currently, D. citri can be found in all citrus growing US states; i.e. Alabama, Arizona, California, Florida, Georgia, Louisiana, Mississippi, South Carolina, Texas, as well as Hawaii (Grafton-Cardwell et al. 2013). In 2005, plants with HLB infection were detected in Florida; within 4 years, all 32 citrus growing counties in the state had HLB-infected citrus (Grafton-Cardwell et al. 2013). HLB is considered the most destructive disease of citrus crops in the world. All known citrus cultivars are susceptible to HLB (Folimonova et al. 2009), and prevention of disease transmission has proven difficult worldwide (Grafton-Cardwell et al. 2013). Infected young trees can die before they reach the fruit bearing stage (Grafton-Cardwell et al. 2013). Infected mature trees decline and can die within 5-10 years of infection, if not managed with enhanced nutrition. Before their demise, infected mature trees produce a portion of fruit that are unmarketable; these fruit are small, misshapen, with uneven color development or remain green. Juice from infected fruit tastes bitter and unbalanced due to low soluble solids and high acid contents. Given effective pathogen acquisition and transmission capabilities of D. citri (Pelz-Stelinski et al. 2010) aided by short (Boina et al. 2009a) and long-range dispersal capabilities, HLB spreads rapidly within and between groves. Continuous 30 min feeding by healthy D. citri on an HLB-infected host plant is necessary for acquisition of the bacterium (Grafton-Cardwell et al. 2013). Once the D. citri acquires the bacterium, a latent period ranging from 7-25 days may exist before the D. citri is able to transmit bacteria into another host plant (Pelz-Stelinski et al. 2010). Time periods involved in acquisition, latency and transmission provide a window of opportunity for controlling infected D. citri and preventing disease spread. Gravid D. citri females lay eggs only on new flush, and early instar nymphs feed on new flush and go through five instars before becoming adults. This results in very high buildups of D. citri populations during flushing periods that are capable of acquiring and transmitting HLB bacteria. Furthermore, within perennially growing citrus in sub-tropical climates, multigenerational and season-long occurrence of arthropod pests, such as D. citri, is common. The problem of insecticide resistance development in citrus is a recurrent worldwide problem and has been well documented. Soil and foliar applied insecticides play a vital role in suppressing D. citri populations (Srinivasan et al. 2008; Boina et al. 2009b) that are infected or capable of acquiring and transmitting HLB bacteria. There is currently only one mode of action (neonicotinoids) available as a soil-applied, systemic treatment for control of D. citri; a situation that will encourage rapid development of resistance. Neonicotinoids are the most widely used insecticides for protecting newly planted groves or young tree resets. After trees come into production, foliar applications are implemented. Conventional spray application methods of high volume airblast sprays of >100 gallons per acre are often insufficient to manage the need for 8-12 applications that target D. citri alone. Control of D. citri to suppress HLB incidence costs growers an additional $1,000 or more per acre each year (Muraro 2009). Given the extra expense, an optimized spray delivery method for these additional D. citri applications is a must for the US citrus industry (Grafton-Cardwell et al. 2013). In response, low volume, ‘misting’ based on cold fogging technology was widely investigated in Florida citrus and has now become widely accepted by the Florida citrus industry (Grafton-Cardwell et al. 2013). Given the mobility of D. citri, HLB has rapidly spread in Florida despite efforts to control the disease (Boina et al. 2009a; Tiwari et al. 2010). D. citri adults disperse long distances during periods of peak activity and move the causal pathogen of HLB widely; particularly from unmanaged, abandoned areas into well managed groves (Tiwari et al. 2010). Grower neighbors often made independent decisions on production and pest management, and these tendencies are being overcome through outreach and demonstrations of the benefits of cooperative actions. A spray program effectively applied to a single block of citrus and not to neighboring blocks will be ineffectual, as untreated blocks serve as sources of infected D. citri and disease (Tiwari et al. 2010). Thus, it has become clear that area-wide, cooperative management of the vector has been necessary. Recently, the US National Academy of Science published a strategic plan for management of HLB and identified development and implementation of area-wide, cooperative so-called “Citrus Health Management Areas (CHMAs)” as the most important organizational priority for HLB management (National Research Council 2010). Significant progress has been made to develop these CHMAs and many already exist (www.flchma.org) (Rogers et al. 2012). Existing CHMAs will continue to improve in Florida and throughout the US in effectiveness and new ones will become established as new D. citri management strategies are developed. While D. citri is the main focus of this project, based on what is described above, other insect pests of Florida citrus (and other crops) will also be investigated to develop management strategies for multiple pests. What opportunities for training and professional development has the project provided? Graduate students have been trained. Foreign interns have been trained. Citrus grower clientele in Florida, the U.S., and international have been trained. How have the results been disseminated to communities of interest? Yes, the reuslts have been disseminated in major citrus growing regions in the United States and Abroad through peer reviewed publication, workshop presentations, extension documents, and direct visits. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? I have developed a program for evaluating new tools (experimental or currently unregistered pesticides) for management of key citrus pests and extend this information to growers and the pesticide industry in an efficient manner. I have focused a significant amount of my efforts on Asian citrus psyllid and citrus leafminer given the current needs of the industry, but have also actively pursued extension activities on other important pests, such as the Diaprepes root weevil. A large part of this program has been dedicated to educating growers on the use of low volume pesticide applications for control of Asian citrus psyllid. My extension and research programs have been intimately linked to produce measurable outcomes for improved citrus production. They have significantly contributed to the adoption and wide use of low volume pesticide spray technologies for management of Asian citrus psyllid in Florida. Low volume pesticide sprayers deliver 2-10 gallons of spray volume per acre and are thus able to cover many more acres of crop per hour, at a lower cost, than conventional pesticide sprayers. As a direct impact, my research and closely associated extension efforts significantly contributed to the issuing of four 24(c) (special local needs) labels to allow use of these products (Danitol, Mustang, Delegate, and Micromite) for Asian citrus psyllid management with low volume sprayers in Florida citrus. Following this progress in Florida, other researchers and extension personnel in Texas have educated citrus growers in that state regarding this technology for management of Asian citrus psyllid. Adoption of low volume technology in Texas for psyllid control is thus also beginning. Since this new use pattern of low volume application has become established for Asian citrus psyllid management in Florida, a significant portion of my extension program has continued to focus on educating growers on how to implement low volume spray technologies optimally, safely, and according to the law. Much of this extension effort has been based on the research findings of my laboratory and the laboratories of Drs. M. Salyani and M. Rogers from UF-CREC and Dr. P. Stansly from the UF-SWFREC. Partially based on my efforts, this technology is now widely adopted among the Florida citrus industry. Low volume application technology requires 1/3rd of the investment of conventional airblast spraying for ACP control. As a direct impact, it has been estimated by economists focusing on citrus production that adoption of low volume ground technology as a component of Asian citrus psyllid management (beginning ca. 2009) by Florida citrus growers is saving the industry at least $40 million per year. My combined research and extension program on the biology of key citrus pests has also contributed to state-wide change in behavior regarding the problem of abandoned citrus groves in Florida. Currently, there are nearly 140,000 acres of abandoned citrus in Florida. My research program has clearly demonstrated that these abandoned groves have a negative impact on commercial citrus production by contributing to the introduction of pests and disease into adjacent managed areas. The integration of my research and extension programs has led to changes in behavior including removal of these unmanaged, abandoned areas or site-specific management, such as a focus on border rows, for those growers who are adjacent to these problem areas. Another direct impact of this extension effort is its contribution to the addition of several new recommendations for pest management to the Florida Citrus Pest Management Guide (use patterns for Delegate WG, Movento 240 SC, Mustang Max, Sevin XLR, and Intrepid 2F). Also, a direct result of my effort has been a 24(c) (special local needs) label for use of Intrepid 2F insecticide against citrus leafminer in Florida citrus. My current efforts include educating growers on the use of this new tool for this important pest of citrus. The remaining portion of my effort in this program focuses on continued education of growers on optimal citrus pest management based on the recommendations set forth by the citrus research and extension team in the Florida Citrus Pest Management Guide. My research and extension efforts in this area have directly resulted in the registration of a pheromone-based mating disruption product (SPLAT-CLM) manufactured and distributed by ISCA Technologies for control of citrus leafminer in Florida citrus. This is a pesticide alternative control tool that protects crops by preventing mating rather than deploying a toxicant. The 24(c) (special local needs) label was approved in April of 2010 with the assistance of my extension and research efforts on this topic. The product currently is fully labeled for use in Florida. My extensive statewide grower education program regarding the proper use of mating disruption for citrus leafminer is resulting in use of this technology by some growers for control of this important pest. To my knowledge, this is the first pesticide alternative product to be developed, registered, and in the early stages of adoption for control of citrus leafminer in Florida and elsewhere. As adoption of this pest-specific and otherwise harmless (to the environment and non-target organisms) product may increase, the negative impact of conventional pesticides (environmental contamination, killing of beneficial insects, pesticide resistance) should be reduced. Furthermore, my efforts in this program have increased the use of pheromone traps for citrus leafminer monitoring as well as monitoring of the Asian citrus psyllid by Florida citrus growers. Grower adoption of pest monitoring should improve efficiency of pest management by allowing growers to better evaluate and time their annual treatments. This program has also contributed to educating growers on the correct use of pesticides, including appropriate rotation of available modes of action, in an effort to minimize development of pesticide resistance. Our monitoring efforts of pesticide susceptibility levels of Asian citrus psyllid to date have revealed only very low levels of resistance development to certain pesticides, and we plan to maintain these low levels with continued monitoring and grower education. Also, our continued monitoring efforts have shown that by 2012, the levels of resistance to some of the most important insecticides for Asian citrus psyllid management (neonicotinoids) have actually decreased as compared with previous years. It is possible that these positive trends are to some degree due to grower adoption of the insecticide-rotation methods and education that my program has contributed to.

Publications

  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Tiwari, S. and L.L. Stelinski. 2013. Effects of cyantraniliprole, a novel anthranilic diamide insecticide, against Asian citrus psyllid under laboratory and field conditions. Pest Management Science. 69: 1066-1072. Martini, X., T. Addison, B. Fleming, I. Jackson, K. Pelz-Stelinski, and L.L. Stelinski. 2013. Occurrence of Diaphorina citri (Hemiptera: Liviidae) in an unexpected ecosystem: The Lake Kissimmee state park forest, Florida. Florida Entomologist. 96: 658-660. Mann, R.S., R.L. Rouseff, J. Smoot, C.N. Rao, W.L. Meyer, S.L. Lapointe, P.S. Robbins, D. Cha, C. Linn, F.X. Webster, S. Tiwari, and L.L. Stelinski. 2013. Chemical and behavioral analysis of the cuticular hydrocarbons from Asian citrus psyllid, Diaphorina citri. Insect Science. 20: 367-378. Tiwari, S., N. Killiny, R.S. Mann, E.J. Wenninger, and L.L. Stelinski. 2013. Abdominal color of the Asian citrus psyllid, Diaphorina citri, is associated with susceptibility to various insecticides. Pest Management Science. 69: 535-541. Stelinski, L. and S. Tiwari 2013. Vertical T-maze choice assay for arthropod response to odorants. Journal of Visualized Experiments. (72), e50229, doi:10.3791/50229. Tiwari, S., Killiny, N., and L.L. Stelinski. 2013. Dynamic insecticide susceptibility changes in Florida populations of Diaphorina citri (Hemiptera: Psyllidae). Journal of Economic Entomology. 106: 393-399. Stelinski, L.L., L.J. Gut, and J.R. Miller. 2013. An attempt to increase efficacy of moth mating disruption by co-releasing pheromones and kairomones and to understand possible underlying mechanisms of this technique. Environmental Entomology. 42: 158-166. Grafton-Cardwell, E., L.L. Stelinski, and P.A. Stansly. 2013. Biology and management of Asian citrus psyllid, vector of huanglongbing pathogens. Annual Review of Entomology. 58: 413-432.


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

Outputs
OUTPUTS: In 2012, I authored or co-authored 11 peer-reviewed articles journals spanning several disciplines. This includes a high impact paper in PloS Pathogens that has already received significant attention and was cited three times in the same year of publication. This also includes two papers in Plos ONE and one in Journal of Chemical Ecology that have also received either media attention or have been cited in the same year of publication. Also, I have several accepted/in press papers or with volume and page numbers for 2013. In addition, in 2012, I co-authored one non-refereed scientific journal proceedings article. Furthermore, I co-authored four contributed presentations at a national scientific meeting. I also presented two national invited talks (during two separate symposia at the national ESA meeting). I processed and edited many papers as Associate Editor of Florida Entomologist and Environmental Entomology. I reviewed many manuscripts in 2012 for several journals spanning many disciplines. My extension program continues to focus on development of educational tools and dissemination of information about 1) Integrated pest management strategies for Florida citrus, and 2) Judicious use of pesticides including pesticide alternative tools, monitoring, resistance management, and pesticide application technologies. I also assist the core extension management team regularly. I have also become involved in statewide extension programs dealing with ambrosia beetles in a small role. The goals and accomplishments of my extension program are described in depth below. By the numbers, in 2012, I presented 8 extension talks to groups of growers, production managers, or industry personnel. Also, I authored 3 trade journal articles in Citrus Industry Magazine. PARTICIPANTS: Collaborators included scientists from the USDA-ARS, pesticide industry, as well as the pesticide alternatives industry. TARGET AUDIENCES: Fruit growers, particularly citrus growers in the USA. PROJECT MODIFICATIONS: Not relevant to this project.

Impacts
My research program in 2012 focused primarily on citrus pest management, and fundamental aspects of insect and nematode behavior and chemical ecology. In 2012, in collaboration with USDA-ARS, I made further progress on refinement and practical application of mating disruption for citrus leafminer. For this work, I received the Annual Achievement Award for Team Research from the Florida Entomological Society (Jointly with USDA-ARS, Fort Pierce). Although a useful and commercially available product now exists, improved formulations and devices will be available next year based on our research in 2012. My lab has made further progress on development of psyllid repellents and attractants for Asian citrus psyllid. Some of this work has recently been published early online or is in print in journals described below and I am making progress with Bayer Crop Science, as well as, other companies and colleagues to deliver practical products (psylid lures an repellents) for use in the field. My laboratory produced a large amount of fundamental work on the behavior of Asian citrus psyllid and psyllid-pathogen-plant interactions in 2012. Briefly, we elucidated how pathogen infection alters plant volatile release so as to attract psyllid deceptively to plant of sub-optimal nutritional status. This may serve as a mechanism to promote pathogen spread (paper in PloS Pathogens). Also, we identified a specific chemical released by citrus roots that attracts a broad range of beneficial nematode species in commercial citrus and blueberry (paper in PLoS ONE) and we collaborated in identifying a nematode pheromone that causes plant parasitic nematodes to disperse and thus could be used as a methyl bromide alternative for plant protection (paper in PLoS ONE). We also elucidated the biochemical basis of organophosphate and carbamate resistance in Asian citrus psyllid, which should aid in developing effective resistance management programs (paper in Journal of Economic Entomology). We also identified several candidate attractants for Asian citrus psyllid from citrus; described the bacterial communities hosted by ambrosia beetle species from across the globe, and described how pheromone exposure affects the mating behavior of female moths across multiple species (various papers cited below). On the more applied side, we further optimized various parameters for low volume insecticide spray applications against Asian citrus psyllid, evaluated the effectiveness of novel semiochemical dispensers that simultaneously release pheromones with plant volatiles for moth mating disruption, and evaluated the effects of insect growth regulators against various developmental stages of Asian citrus psyllid (various papers cited below).

Publications

  • Robbins, P.S., R.T. Alessandro, L.L. Stelinski, and S.L. Lapointe. 2012. Volatile profiles of young leaves of Rutaceae spp. varying in susceptibility to the Asian citrus psyllid (Hemiptera: Psyllidae). Florida Entomologist. 95: 774-776.
  • Hulcr, J., N.R. Roundtree, S.E. Diamonds, L.L. Stelinski, N. Fierer, and R.R. Dunn. 2012. Mycangia of ambrosia beetles host communities of bacteria. Microbial Ecology. 64: 784-793.
  • Tiwari, S., P.J. Clayson, E.H. Kuhns, and L.L. Stelinski. 2012. Effects of buprofezin and diflubenzuron on various developmental stages of Asian citrus psyllid, Diaphorina citri.Pest Management Science. 68:1405-1412.
  • Ali, J.G., H.T. Alborn, R. Campos-Herrera, F. Kaplan, L.W. Duncan, C. Rodriguez-Saona, A.M. Koppenhoefer, and L.L. Stelinski. 2012. Subterranean, herbivore-induced plant volatile increases biological control activity of multiple beneficial nematode species in distinct habitats. PLoS ONE. 7(6): e38146.
  • Kaplan, F., H.T. Alborn, S.H. von Reuss, R. Ajredini, J.G. Ali, F. Akyazi, L.L. Stelinski, A.S. Edison, F.C. Schroeder, and P.E. Teal. 2012. Interspecific nematode signals regulate dispersal behavior. PLoS ONE. 7(6): e38735.
  • Tiwari, S., L.L. Stelinski, and M.E. Rogers. 2012. Biochemical basis of organophosphate and carbamate resistance in Asian citrus psyllid. Journal of Economic Entomology. 105: 540-548.
  • Mann, R.S., J.G. Ali, S.L. Hermann, S. Tiwari, K.S. Pelz-Stelinski, H.T. Alborn, and L.L. Stelinski. 2012. Induced release of a plant defense volatile deceptively attracts insect vectors to plants infected with a bacterial pathogen. PLoS Pathogens. 8(3): e1002610.
  • Kuhns, E.H., K. Pelz-Stelinski, and L.L. Stelinski. 2012. Reduced mating success of female tortricid moths following intense pheromone auto-exposure varies with sophistication of mating system. Journal of Chemical Ecology. 38: 168-175.
  • Knight, A.L., L.L. Stelinski, V. Hebert, L. Gut, D. Light, and J. Brunner. 2012. Novel dispensers simultaneously releasing pear ester and sex pheromone for disruption of codling moth (Lepidoptera: Tortricidae). Journal of Applied Entomology. 136: 79-86.
  • Mann, R.S., S. Tiwari, J.M Smoot, R.L. Rouseff, and L.L. Stelinski. 2012. Repellency and toxicity of plant-based essential oils and their constituents against Diaphorina citriKuwayama (Hemiptera: Psyllidae). Journal of Applied Entomology. 136: 87-96.
  • Boina, D.R., M. Salyani, S. Tiwari, K. Pelz-Stelinski, and L.L. Stelinski. 2012. Spray droplet size affects efficacy of fenpropathrin against Asian citrus psyllid. Pesticide Formulations and Delivery Systems: Innovating Legacy Products for New Uses. ASTM International. STP 1558, pp. 1-13 doi:10.1520/STP104310.


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

Outputs
OUTPUTS: In 2011, I authored or co-authored 17 peer-reviewed articles in high quality journals spanning several disciplines. This is an annual personal best for me. Also, I have several accepted/in press papers or with volume and page numbers for 2012. In addition, in 2011, I had two published abstracts and three submitted provisional patent applications (one of which has been processed). Furthermore, I authored or co-authored one invited as well as, four contributed presentations at international scientific meetings. I co-authored 2 state contributed presentations at scientific meetings (FES); 10 national contributed talks (ESA, etc). I also presented two invited departmental seminars at Cornell University (one to the Department of Entomology in Ithaca and one at the Geneva Agricultural Experiment Station). I also presented two other national invited talks (one in a symposium at the ESA and one at a Texas citrus show). By the numbers, in 2011, I presented or co-authored 4 extension talks to groups of growers, production managers, or industry personal. I also co-authored 2 EDIS papers and 2 trade journal articles. PARTICIPANTS: Not relevant to this project. TARGET AUDIENCES: The target audience has been the applied insect pest management community, basic ecologists, and entomologists. The audience also includes fruit and vegetable growers, focusing on citrus growers. PROJECT MODIFICATIONS: Not relevant to this project.

Impacts
My research program in 2011 focused on citrus pest management, and fundamental aspects of insect and nematode behavior and chemical ecology. In 2011, in collaboration with USDA-ARS, I made further progress on refinement and practical application of mating disruption for citrus leafminer. A useful and commercially available product now exists. In 2011 (also in collaboration with USDA-ARS), I submitted a provisional patent application for a unique chemical compound released by plant roots (examples: citrus, blueberry) upon feeding by insect larvae that attracts entomopathogenic nematodes. Exogenous application of the synthetic chemical increases insect mortality in the soil by attracting beneficial nematodes to areas of beetle infestation. The patent application is now well in process. Also, we identified a dispersal pheromone that is released by nematodes and perceived interspecifically by diverse nematode species. From a practical perspective, it causes plant parasitic nematodes to disperse and thus could be used to repel these cosmopolitan pests from crops and serve as a methyl bromide alternative. My lab made further progress on development of psyllid repellents and I received the Technology Innovator Award from Office of Technology Transfer, University of Florida associated with this work. Also, in terms of applications of chemical ecology, we made further progress with attractants for Asian citrus psyllid. Prior to the end of the year, I submitted two provisional patent applications for psyllid attractants: one for a plant volatile-based lure and one for a pheromone-based lure. These are currently being processed. In 2011, my lab made significant progress in elucidating the biochemical mechanisms of insecticide resistance in Asian citrus psyllid. We determined: 1) the effects of Liberibacter infection on psyllid susceptibility to insecticides; 2) changes in susceptibility levels of psyllid populations over the course of three years; 3) detoxifying enzyme mechanisms responsible for changes in resistance levels; 4) levels of target site insensitivity to organophosphate and carbamate insecticides; and, 5) identified five novel genes associated with resistance to imidacloprid in Asian citrus psyllid. These results are helping us develop appropriate rotations for optimal resistance management and an RNAi-based tool for preventing or reversing imidacloprid resistance is slowly in progress In 2011, we described novel interactions between Asian citrus psyllid and Liberibacter bacteria and a novel transmission mechanism. Specifically, we proved sexual transmission of the bacteria during mating we experimentally showed that infection of plants with the pathogen induces plant responses that modify behavior of the vector so as to proliferate the spread of pathogen. We have also made significant progress elucidating the behavior and ecology of ambrosia beetles, both in terms of fundamental biology and for potential practical application. We are the first to show that ambrosia beetles are attracted to the odors of their fungal symbionts. We are using this information to identify attractants.

Publications

  • Hulcr, J., R.S. Mann, and L.L. Stelinski. 2011. The scent of a partner: Ambrosia beetles are attracted to volatiles from their fungal symbionts. Journal of Chemical Ecology. 37: 1374-1377.
  • Mann, R.S., K. Pelz-Stelinski, S.L. Hermann, S. Tiwari, and L.L. Stelinski. 2011. Sexual transmission of a plant pathogenic bacterium, Candidatus Liberibacter asiaticus, between conspecific insect vectors during mating. PLoS ONE. 6(12): e29197.
  • Youn, Y., E.A. Backus, R.H. Serikawa, and L.L. Stelinski. 2011. Correlation of an electrical penetration graph waveform with walking by Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae). Florida Entomologist. 94: 1084-1087.
  • Tiwari, S., A. Gondhalekar, R.S. Mann, M.E. Scharf, and L.L. Stelinski. 2011. Characterization of five CYP4 genes from Asian citrus psyllid and their expression levels in Candidatus Liberibacter asiaticus infected and uninfected psyllids. Insect Molecular Biology. 20: 733-744.
  • Lapointe, S.L., and L.L. Stelinski. 2011. An applicator for high viscosity semiochemical products and intentional gaps for mating disruption of Phyllocnistis citrella. Entomologia Experimentalis et Applicata. 141: 145-153.
  • Tiwari, S., R.S. Mann, M.E. Rogers, and L.L. Stelinski. 2011. Insecticide resistance in field populations of Asian citrus psyllid in Florida. Pest Management Science. 67: 1258-1268.
  • Sanders, W.R., O.E. Liburd, R.W. Mankin, W.L. Meyer, and L.L. Stelinski. 2011. Applications and mechanisms of wax-based semiochemical dispenser technology for disruption of grape root borer mating. Journal of Economic Entomology. 104: 939-946.
  • Sanders, W.R., R.W. Mankin, O.E. Liburd, and L.L. Stelinski. 2011. Acoustic detection of arthropod infestation of grape roots: scouting for grape root borer (Lepidoptera: Sesiidae). Florida Entomologist. 94: 296-302.
  • Epstein, D.L., J.R. Miller, M.J. Grieshop, L.L. Stelinski, and L.J. Gut. 2011. Direct sampling of resting codling moth (Lepidoptera: Tortricidae) adults in apple tree canopies and surrounding habitats. Environmental Entomology. 40: 661-668.
  • Epstein, D.L., L.L. Stelinski, J.R. Miller, M.J. Grieshop, and L.J. Gut. 2011. Effects of reservoir dispenser height on efficacy of mating disruption of codling moth (Lepidoptera: Tortricidae) in apple. Pest Management Science. 67: 975-979.
  • Tiwari, S., K. Pelz-Stelinski, R.S. Mann and L.L. Stelinski. 2011. Glutathione S-transferase and cytochrome P450 (general oxidase) activity levels in Candidatus Liberibacter asiaticus-infected and uninfected Asian citrus psyllid, Diaphorina citri. Annals of the Entomological Society of America. 104: 297-305.
  • Onagbola, E.O., R.L. Rouseff, J.M Smoot, and L.L. Stelinski. 2011. Guava leaf volatiles and dimethyl disulfide inhibit response of Diaphorina citri Kuwayama to host plant volatiles. Journal of Applied Entomology. 135: 404-414.
  • Lapointe, S.L., L.L. Stelinski, and R.D. Robinson. 2011. A novel pheromone dispenser for mating disruption of the leafminer Phyllocnistis citrella (Lepidoptera: Gracillariidae). Journal of Economic Entomology. 104: 540-547.
  • Ali, J.G., H.T. Alborn, and L.L. Stelinski. 2011. Constitutive and induced subterranean plant volatiles attract both entomopathogenic and plant parasitic nematodes. Journal of Ecology. 99: 26-35.
  • Mann, R.S., R.L. Rouseff, J.M Smoot, W.S. Castle, and L.L. Stelinski. 2011. Sulfur volatiles from Allium spp. affect Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), response to citrus volatiles. Bulletin of Entomological Research. 101: 89-97.
  • Tiwari, S., K. Pelz-Stelinski, and L.L. Stelinski. 2011. Effect of Candidatus Liberibacter asiaticus infection on susceptibility of Asian citrus psyllid, Diaphorina citri, to selected insecticides. Pest Management Science. 67: 94-99.
  • Boina, D.R., Y. Youn, S. Folimonova, and L.L. Stelinski. 2011. Effects of pymetrozine, an antifeedant of Hemiptera, on Asian citrus psyllid, Diaphorina citri, feeding behavior, survival, and transmission of Candidatus Liberibacter asiaticus. Pest Management Science. 67: 146-155.


Progress 10/01/08 to 09/30/09

Outputs
OUTPUTS: Events: Up data on current and future psyllid control strategies. 3 November. Invited talk presented to the "No Names" grower organization in Lake Wales, FL. Controlling the psyllid-current strategies and possible future tools. 20 October. Invited talk presented to the "Ridge Runners" grower organization in Winter Haven, FL. Update on psyllid management: Low volume technology, pesticides, and pesticide alternatives. Citrus Expo. 19th August. Lee Civic Center, Fort Myers, FL. Aerial spray applications for psyllid control. Citrus Expo. 19th August. Lee Civic Center, Fort Myers, FL. Update on low volume spray application technology to manage the citrus psyllid. 23rd June. Extension Seminar, Immokalee IFAS Center in Immokalee, FL. Low volume applications for psyllid management update. West Central Florida Citrus Psyllid Management Update and Demonstration. 19 May. Dade City, FL. Psyllid research at A.H. Krezdorn Grove: Experimental compounds. 14 May. Mid Florida Citrus Foundation field day. Orlando, FL. Psyllid repellent technology. 13 May, Florida Citrus Mutual Tour. CREC, Lake Alfred, FL Low volume technology for Asian citrus psyllid management. Citrus Greening Symposium. 2009 Florida Citrus Growers' Institute, Stuart Conference Center, Bartow, FL. Improving our ability to manage citrus leafminer. 1 April. Florida Citrus Production Manager's Association Meeting. CREC, Lake Alfred, FL. New technologies for managing Asian citrus psyllid. 31 March. Invited talk presented to the "Ridge Runners" grower organization in Winter Haven, FL. Low volume sprays for control of Asian citrus psyllid. Low volume/fogging seminar to manage psyllids. Sponsored by the Highlands County Citrus Growers Association. Bert J. Harris, Jr. Agricultural Center, Highlands County Extension Advisory Committee, Sebring, FL. Citrus leafminer control and low volume sprays. 10th February. Citrus Production School. Turner Exhibition Hall, Arcadia, FL. Psyllid management. 3rdth February. Citrus Production School. Turner Exhibition Hall, Arcadia, FL. Psyllid management update and the impact of abandoned groves Indian River Citrus Seminar. 27th January, Ft. Pierce, FL. SPLAT-CLM: A new product for controlling citrus leafminer and canker. Indian River Citrus Seminar. 27th January, Ft. Pierce, FL. Update on psyllid control research: From pheromones to low volume pesticide applications. 20th January. Highlands County Citrus "OJ Break". Bert J. Harris, Jr. Agricultural Center, Highlands County Extension Advisory Committee, Sebring, FL. The cutting edge on psyllid management. 14th January. Production Managers Meeting, CREC, Lake Alfred, FL. Stelinski, L.L., and M.E. Rogers. 2009. Update on psyllid management given new insights regarding movement and potential new uses of low volume sprays. 14th January. Citrus Research and Education Center. Products: Development of an educational web site for Florida citrus growers on the use of Low volume spray technology for control of Asian citrus psyllid in Florida citrus. Volume Applications: An Emerging Technology in the Citrus Industry. http://www.crec.ifas.ufl.edu/extension/greening/index.htm PARTICIPANTS: Not relevant to this project. TARGET AUDIENCES: Not relevant to this project. PROJECT MODIFICATIONS: Not relevant to this project.

Impacts
Over the past year, we have been working to develop an effective repellent for the Asian citrus psyllid (ACP). Our work was initiated by investigating the volatiles released by guava plants and their effects on ACP behavior. Following the discovery that synthetic dimethyl disulfide (DMDS) was produced in large quantities by wounded guava leaves, we initiated an investigation of the effects of this chemical on ACP behavior. DMDS is a known plant defense chemical against insects that acts as both a repellent and a neurotoxin. In laboratory tests, we have confirmed that volatiles from guava leaves significantly inhibited ACP's response to normally attractive citrus host-plant volatiles. A similar level of inhibition was recorded when synthetic DMDS was co-released with volatiles from citrus leaves. Compounds similar to DMDS including dipropyl disulfide, ethyl-1-propyl disulfide, and ethyl disulfide did not affect the behavioral response of ACP to attractive citrus host plant volatiles in laboratory behavioral tests. These data suggest that the activity of DMDS on the behavior of ACP is unique and not shared by all disulfide compounds. However, more recently we have found that another sulfur compound, dimethyl trisulfide, is slightly more active against the psyllid than the originally identified DMDS. Our current on-going efforts include formulating DMDS into controlled release devices for extended release of the chemical in the field. Control of ACP with behavioral modification may be one potential tool for management of this plant disease vector. Research has continued on the development of effective control tools for the citrus leafminer (CLM). One of the main thrusts of this project has been to develop pheromone based control strategies for this pest that will serve as alternatives to broad-spectrum insecticides and that should be comparable or better than insecticides in terms of efficacy and cost. Most recently, we developed and evaluated an attract-and-kill formulation, termed MalEx, for control of CLM. MalEx is a viscous paste with UV-protective properties that is dispensed as small (50 μl) droplets using custom-made calibrated pumps. Continuous treatment of 1.2 acre blocks of citrus with MalEx over the course of 112 d reduced larval infestation of new leaf flush by 3.6-7.2 fold. Control of CLM with MalEx should reduce the number of required broad spectrum sprays for leafminer management in both field and citrus nursery settings. For our ongoing mating disruption studies, we have determined the most effective dosage of pheromone and blend of pheromone components for CLM control. This work has been conducted with an industry collaborator (ISCA Technologies, Inc.) who is developing and registering a pheromone product named SPLAT for CLM management in Florida. The SPLAT-CLM formulation consistently reduces leafmier infestation and population densities.

Publications

  • Rodriquez Saona, C. and L.L. Stelinski. 2009. Behavior modifying strategies in IPM Theory and Practice, In: R. Peshin and A.K. Dhawan (eds.) Integrated Pest Management: Innovation, Development Process. Springer, NY. pp. 261-311.
  • Lapointe S.L., L.L. Stelinski, T.J. Evens, R.P. Niedz, D.G. Hall, and A. Mafra-Neto. 2009. Sensory imbalance as mechanism of orientation disruption in the leafminer Phyllocnistis citrella: elucidation by multivariate geometric designs and response surface models. Journal of Chemical Ecology. 35: 896-903.
  • Boina, D.R., W.L. Meyer, E.O. Onagbola, and L.L. Stelinski. 2009. Quantifying dispersal of Diaphorina citri (Hemiptera: Psyllidae) by immunomarking and potential impact of unmanaged groves on commercial citrus management. Environmental Entomology. 38: 1250-1258.
  • Stelinski, L.L., A. Zhang, E.O. Onagbola, and W.L Meyer. 2009. Recognition of foreign oviposition marking pheromones is context dependent and determined by preimaginal conditioning. Communicative and Integrative Biology. 2: 391-393.
  • Huang, J., L.L. Stelinski, J.R. Miller, and L.J. Gut. 2009. Attraction and fecundity of adult codling moth, Cydia pomonella as influenced by methoxyfenozide-treated electrostatic powder. Journal of Applied Entomology. 133: 666-672.
  • Trivedi, P., U.S. Sagaram, J.-S. Kim., R.H. Brlansky, M.E. Rogers, L.L. Stelinski, C. Oswalt, and N. Wang. 2009. Quantification of viable Candidatus Liberibacter asiaticus in hosts using quantitative PCR with the aid of ethidium monoazide (EMA). European Journal of Plant Pathology. 124: 553-563.
  • Onagbola, E.O., D.R. Boina, S.L. Herman, and L.L. Stelinski. 2009. Antennal sensilla of Tamarixia radiata (Hymenoptera: Eulophidae), a parasitoid of Diaphorina citri (Hemiptera: Psyllidae). Annals of the Entomological Society of America. 102: 523-531.
  • Stelinski, L.L., C. Rodriguez-Saona, W. Meyer, and A. Zhang. 2009. Recognition of parasitoid oviposition deterring pheromones by their fruit fly hosts. The fifth Asia-Pacific Conference on Chemical Ecology. 26-30th October, Honolulu, Hawaii. Page 47.
  • Lapointe, S., and L.L. Stelinski. 2009. Pheromones as mixtures: Geometric designs and response surface modeling for optimization of mating disruption of the citrus leafminer Phyllocnistic citrella. The fifth Asia-Pacific Conference on Chemical Ecology. 26-30th October, Honolulu, Hawaii. Page 96.
  • Stelinski, L.L. 2009. Controlling the psyllid. Guava volatiles and other remedies. The 49th Annual International Citrus & Beverage Conference. 15-18 September, Clearwater Beach, FL. Page 22.
  • Forbes, A.A., H.Q. Powell, L.L. Stelinski, J.J. Smith, and J.L. Feder. 2009. Sequential sympatric speciation across trophic levels. Science. 323: 776-779. Boina, D.R., E.O. Onagbola, M. Salyani, and L.L. Stelinski. 2009. The influence of post-treatment temperature on the toxicity of insecticides against Asian citrus psyllid, Diaphorina citri, Kuwayama. Journal of Economic Entomology. 102: 685-691.
  • Stelinski, L.L., C. Rodriguez-Saona, and W.L. Meyer. 2009. Recognition of foreign oviposition marking pheromone in a multitrophic context. Naturwissenschaften. 96: 585-592.
  • Gokce, A., L.L. Stelinski, M.E. Whalon, and L.J. Gut. 2009. Toxicity and antifeedant activity of selected plant extracts against larval obliquebanded leafroller, Choristoneura rosaceana (Harris). The Open Entomology Journal. 3: 30-36.
  • Stelinski, L.L., A.L. IlIchev, and L.J. Gut. 2009. Efficacy and release rate of reservoir pheromone dispensers for simultaneous mating disruption of codling moth and oriental fruit moth (Lepidoptera: Tortricidae). Journal of Economic Entomology. 102: 315-323.
  • Boina, D.R., M. Salyani, and L.L. Stelinski. 2009. Chemical control of the Asian citrus psyllid, Diaphorina citri Kuwayama. Proc. Fla. State Hort. Soc. In press.
  • Boina, D.R., M.E. Rogers, and L.L. Stelinski. 2009. Resistance of Asian citrus psyllid to pesticides. Citrus Industry Magazine. 90(9): 14-15, and 21.
  • Stelinski, L.L., M.E. Rogers, and S. Lapointe. 2009. Citrus leafminer mating disruption. Citrus Industry Magazine. 90(7): 8-9.
  • Atwood, R., and L.L. Stelinski. 2009. A citrus research jewel: the A.H. Krezdorn grove; experiments aimed at psyllids, leafminers, and weeds. Citrus Industry Magazine. 90(5): 18-21.
  • Gut, L.J., J. Miller, P. McGhee, D. Epstein, and L. Stelinski. 2009. Pheromone-based approaches to manage pests. Fruit Grower News. March Issue.
  • Rogers, M.E., and L.L. Stelinki. 2009. Development of new tools and recommendation for psyllid management programs. Citrus Industry Magazine. 90(1): 8-10.
  • Boina, D.R., E.O. Onagbola, M. Salyani, and L.L. Stelinski. 2009. Antifeedant and sublethal effects of imidacloprid on Asian citrus psyllid, Diaphorina citri. Pest Management Science. 65: 870-877.
  • Szendrei, Z., E. Malo, L.L. Stelinski, and C. Rodriguez-Saona. 2009. Response of cranberry weevil (Coleoptera: Curculionidae) to host plant volatiles. Environmental Entomology. 38: 861-869.


Progress 10/01/07 to 09/30/08

Outputs
OUTPUTS: The output of this project has been diseminated widely through industry publications, extension publications, and extention meetings. These findings have also been deseminated in local and national professional society meetings. Three invited presentations were given in 2007 and eight invited presentations were given in 2008 at local field days, work shops, and expos. Also, four national talks were contributed during 2007-2008. Also, a product directly from my research work in 2008 has resulted in a patent application for sulfer compounds identified in Guava as repellents of the Asian citrus psyllid PARTICIPANTS: Michael Rogers, Erik Wenninger, David Hall, Ebenezer Onagbola, Raj Boina, James Miller, Larry Gut, Peter McGhee TARGET AUDIENCES: The Florida and U.S Citrus Industry, County Florida Extension Agents, The Scientific Community PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
My findings have resulted in a substantial change in knowledge regarding use of behavior-modyfying chemicals for insect pest control in citrus. This should lead to the increased use of semiochemicals for pest control in Florida citrus, reducing growers' relliance on broad-spectrum pesticides. Also, my research has resulted in substantial change in action based on the outcomes generated in my lab. Growers are adopting the most effective psyllid control tactics currently available (correct use of pesticides, apporproaite pest monitoring) based on the research results we are providing them with. Finally, my findings have also resulted in a substantial change in knowledge regarding pesticide application technologies, which should soon lead to increased use of more effective and less expensive low volume application technology for Asian citrus psyllid control.

Publications

  • Stelinski, L.L., and L.J. Gut. 2008. Delayed mating in tortricid leafroller species: simultaneously aging both sexes prior to mating is more detrimental to female reproductive potential than aging either sex alone. Bulletin of Entomological Research. In press.
  • Stelinski, L.L., J.R. Miller, and M.E. Rogers. 2008. Mating disruption of citrus leafminer mediated by a non-competitive mechanism at a remarkably low pheromone release rate. Journal of Chemical Ecology. 34: 1107-1113.
  • Stelinski, L.L., P. McGhee, M. Grieshop, J. Brunner, and L.J. Gut. 2008. Efficacy and mode of action of female-equivalent dispensers of pheromone for mating disruption of codling moth, Cydia pomonella (L.). Agricultural and Forest Entomology. 10: 389-397.
  • Wenninger, E.J., L.L. Stelinski, and D.G. Hall. 2008. Behavioral evidence for a female-produced sex attractant in Diaphorina citri. Entomologia Experimentalis et Applicata. 128: 450-459.
  • Stelinski, L.L. and M.E. Rogers. 2008. Factors affecting captures of male citrus leafminer, Phyllocnistis citrella, in pheromone-baited traps. Journal of Applied Entomology. 132: 143-150.
  • Witzgall, P., Stelinski, L. Gut, and D. Thomson. 2008. Codling moth management and chemical ecology. Annual Review of Entomology. 53: 503-522.
  • Stelinski, L.L. 2007. On the physiological and behavioral mechanisms of pheromone-based mating disruption. Pesticides. 3-4: 27-32.
  • Wenninger, E.J., L.L. Stelinski, and D.G. Hall. 2009. The roles of olfactory cues, visual cues, and mating status in orientation of Diaphorina citri Kuwayama (Hemiptera: Psyllidae) to four different host plants. Environmental Entomology. In press.
  • Wenninger, E.J., L.L. Stelinski, and D.G. Hall. 2009. Relationships between adult abdominal color and reproductive potential in Diaphorina citri (Hemiptera: Psyllidae). Annals of the Entomological Society of America. In press.
  • Rouseff, R.L., E.O. Onagbola, J.M. Smoot, and L.L. Stelinski. 2008. Sulfur volatiles in guava (Psidium guajava L.) leaves: possible defense mechanism. Agricultural and Food Chemistry. 56: 8905-8910.
  • Onagbola, E.O., W.L. Meyer, D.R. Boina, and L.L. Stelinski. 2008. Morphological characterization of the antennal sensilla of the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), with reference to their probable functions. Micron. 39: 1184-1191.
  • Mercader, R.J., L.L. Stelinski, and J.M. Scriber. 2008. Differential antennal sensitivities of the generalist butterflies Papilio glaucus and P. canadensis to host plant and non-host plant extracts. Journal of the Lepidopterists Society. 62: 84-88.
  • Stelinski, L.L., D. McKenzie, L.J. Gut, R. Isaacs, and J. Brunner. 2007. Comparison of female attractiveness and male response among populations of Choristoneura rosaceana (Harris) in western and eastern U.S. apple orchards. Environmental Entomology. 36: 1032-1039.
  • Stelinski, L.L., L.J. Gut, M. Haas, P. McGhee, and D. Epstein. 2007. Evaluation of aerosol devices for simultaneous disruption of sex pheromone communication in Cydia pomonella and Grapholita molesta (Lepidoptera: Tortricidae). Journal of Pest Science. 80: 225-233.
  • Stelinski, L.L., P. McGhee, M. Haas, A.L. IlIchev, and L. J. Gut. 2007. Sprayable microencapsulated sex pheromone formulations for mating disruption of four tortricid species: Effects of application height, rate, frequency, and sticker adjuvant. Journal of Economic Entomology. 100: 1360-1369.
  • Stelinski, L.L., R. Oakleaf and C. Rodriguez-Saona. 2007. Oviposition-deterring pheromone deposited on blueberry fruit by the parasitic wasp, Diachasma alloeum. Behaviour. 144: 429-445.
  • Stelinski, L.L., J.R. Miller, R. Ledebuhr, P. Siegert, and L.J Gut. 2007. Season-long mating disruption of Grapholita molesta (Lepidoptera: Tortricidae) by one machine application of pheromone in wax drops (SPLAT-OFM). Journal of Pest Science. 80: 109-117.
  • Gokce, A., L. L. Stelinski, L. J. Gut, and M. E. Whalon. 2007. Comparative behavioral and EAG responses of female obliquebanded and redbanded leafroller moths (Lepidoptera: Tortricidae) to their sex pheromone components. European Journal of Entomology. 104: 187-194.