Progress 10/01/20 to 09/30/21
Outputs
Target Audience:Citrus and avocado growers and industries related to these specialty crops. Changes/Problems:None. What opportunities for training and professional development has the project provided?One of my PhD students, Benita Shrestha, who worked on interactions of Asian citrus psyllid with natural enemies successfully graduated in December of 2021. Also, one of the MS students I co-advised with L. Diepenbrock successfully graduated in September of 2021. Currently, I am co-advising one PhD student (David Olabiyi) and one Masters students (Lourdes Perez) with Lauren Diepenbrock. David is working on aspects of Lebbeck mealybug biology and management. Lourdes is working on repellents for Asian citrus psyllid. I also serve on the PhD committees of Gagandeep Kaur (Entomology- GCREC), Emilie Demard (Entomology-IRREC), Mohamed Ali (Entomology-SWREC), Derrick Conover (Entomology-NFREC), Nicholas Johnston (Entomology-NFREC), and John Ternest (Entomology-Gainesville). In addition, I serve as member on the committee of one entomology Masters student (Rowda Altamimi) at NFREC. How have the results been disseminated to communities of interest?My extension program focuses on development and delivery of statewide educational efforts in citrus pest management with the focus on optimizing the profitability and sustainability of citrus production with the following goals: 1) Changing grower behavior to maintain integrated pest management tactics in citrus under conditions of chronic disease(s) reducing yield and 2) Changing grower behavior to overcome insecticide resistance development. The goals and accomplishments of my extension program are described in depth in the abbreviated T&P packet below. In 2021, I delivered a presentation at the Florida Citrus Show, one presentation at the UF IFAS Florida Citrus Growers' Institute (presented virtually), and one at the Citrus Expo. I also co-organized and presented during a webinar organized by Science for Citrus Health in cooperation with UC Agriculture and Natural Resources. I also presented at the Avocado Laurel Wilt-Ambrosia Beetle Workshop in 2021 and developed a training lecture for the FL Certified Crop Advisor program. By the numbers, in 2021, I developed/presented 6 extension talks to groups of growers, production managers, or industry personnel in Florida and elsewhere. Also, I authored or co-authored one article in Citrus Industry Magazine. I also engaged in several phone call consultations as part of my extension responsibility. I also participated in the revision of three EDIS publications in 2021. What do you plan to do during the next reporting period to accomplish the goals?My 2022 research program will focus on meeting the goals of two existing USDA-SCRI-CDRE projects and one USDA-APHIS-MAC project, which is coming to an end. My intention is to also continue to garner new funding for the lab. Specific areas of current research: Title: Field implementation of an advanced multimodal attract-and-kill device (CAPUT trap) for sustainable management of Asian citrus psyllid. Source: USDA-APHIS-MAC. Purpose: Continue development of attract-&-kill device as a tool for ACP population suppression. Title: Optimal Bt toxins and gene silencing RNAs for management of Asian citrus psyllid to mitigate impact of citrus greening. Source: USDA-NIFA. Purpose: Develop engineered citrus expressing Bt toxin for management of ACP. Combine with RNAi to mitigate resistance development and increase efficacy. Title: Targeting ACP gut to prevent transmission of HLB pathogen. Develop methods and protocols for reducing transmission of the CLas pathogen by the psyllid vector. My role in this project is to develop an extension component. I will be advising 2 graduate students during 2022. I will also serve on committees of 7 other graduate students. I expect that my extension role in the Florida citrus industry will continue at its current pace in both materials produced and impact. I will continue to work with all of the county extension agents focusing on citrus and continue educating growers about my research and the research of my colleagues at CREC, IFAS, and other institutions. I expect that I may be invited to contribute presentations at annual venues, as well as smaller meetings and in-service training. I will continue serving as one of the go-to people regarding psyllid management, psyllid biology/ecology, as well as pyllid control with pesticide alternatives. I will also continue to be one of the go-to entomologists regarding other current insect pests such as the citrus leafminer, Diaprepes root weevil, and Lebbeck mealybug. I have developed a well-known extension role as educator of integrated management strategies, insect ecology, and insecticide resistance. I will continue to distribute new information through publication in appropriate extension outlets such as trade journals or EDIS.
Impacts
What was accomplished under these goals?
A large project that came to an end in 2021 dealt with evaluating economic thresholds to increase sustainability of Asian citrus psyllid (ACP) management in citrus under conditions of high huanglongbing (HLB) incidence. We investigated efficacy of nominal thresholds by relating ACP densities to cost of application and yield. This was overlaid with a comparison of two spray programs in an effort to evaluate the need for an effective dormant season spray and to combine integrated pest management (IPM) with integrated resistance management (IRM) practices. The highest yield was observed with a 0.2 ACP / tap threshold that required 7 annual sprays, while reducing the number of sprays to 5 and below with higher thresholds caused a significant decline in yield. The estimated profit obtained with using the 0.2 ACP / tap threshold was higher than with the two higher thresholds tested, indicating that reducing sprays below 7 per year compromised yield. Susceptibility of ACP to insecticides was monitored and all threshold programs effectively mitigated resistance. Our results indicate that ACP management is most critical during the period between January to March, when citrus is characterized by flowering, fruit maturation (final stage), and the need for safe harvesting. An effective dormant season insecticide spray targeting both adult and immature psyllids near budbreak of the first seasonal flush was required in order to implement a low (0.2 psyllds / tap) treatment threshold during the remainder of the season. A second aspect of CRDF funded research completed in 2021 focused the underlying reasons why biological control does not seem to contribute to management of ACP in Florida even though insecticide inputs have been reduced over the past 5 years. Although biological control is unlikely to impact ACP populations sufficiently to reduce pathogen transmission, it could impact yield indirectly by contributing to population suppression of psyllids below a measurable action threshold discussed above. Collectively, we found that intraguild competition was not a major limiting factor on biological control of ACP. Our results suggested that precision timing of insecticide use limiting sprays to key times when psyllids reach damage thresholds or outbreak levels associated with citrus flush phenology may to help conserve natural enemies. Furthermore, our results suggested that provisioning predators of ACP with additional or supplemental nutrition may be needed to improve their functional response under conditions of prevalent HLB. Finally, incorporation of targeted ant exclusion was the single biggest factor to increase predation of ACP. Our work on the behavioral and chemical ecology of nematodes continues. Most recently, my lab has been involved in research in potato and tomato systems with collaborator Javaad Kirimi. Recently, we demonstrated that entomopathogenic nematodes (EPNs): 1) induce plant defense responses, 2) reduce plant parasitic nematode (PPN) infestation belowground, and 3) reduce herbivore host preference and performance (survival) aboveground. We also showed that these plant responses to EPNs are remarkably similar to those caused by PPNs. Additional results support a pattern indicating that both EPNs and PPNs activate immune response in plants and salicylic acid-regulated defenses. The specific immunity related receptor complexes and signaling pathways are similar when plant roots interact with each nematode functional guild. Therefore, plants may at first recognize EPNs as pathogens and react by activating SAR. In general, populations of PPNs are known to decline upon exogenous applications of EPNs as part of augmentation biological control treatments. We think that the antagonistic effect of EPN on the plant parasitic guilds of nematodes is mediated indirectly via induced systemic acquired resistance in plants. Collective evidence from our study (and others) suggests that plants mistake EPNs as PPNs and respond with induced defense. The mechanism(s) by which plants recognize nematodes to induce SAR are poorly understood; however, ascaroside pheromones produced and released by all functional guilds of nematodes are likely candidates.
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2021
Citation:
Chen, X.D., S. Neupane, T.A. Gill, H. Gossett, K.S. Pelz-Stelinski, and L.L. Stelinski. 2021. Comparative transcriptome analysis of thiamethoxam susceptible and resistant Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), using RNA-sequencing. Insect Science. 28: 1708-1720.
- Type:
Journal Articles
Status:
Published
Year Published:
2021
Citation:
Haghighi, S.R, V. Hosseininaveh, K. Talebi, R. Maali-Amiri and L.L. Stelinski. 2021. Salicylic acid induced resistance in drought-stressed pistachio seedlings influences physiological performance of Agonoscena pistaciae (Hemiptera: Aphalaridae). Journal of Economic Entomology. 114: 2172-2188.
- Type:
Journal Articles
Status:
Published
Year Published:
2021
Citation:
Chen, X.-D., N. Kaur, D.R. Horton, W.R. Cooper, J.A. Qureshi, and L.L. Stelinski. 2021. Crude extracts and alkaloids derived from Ipomoea-Periglandula symbiotic association cause mortality of Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae). Insects. 12, 929.
- Type:
Journal Articles
Status:
Published
Year Published:
2021
Citation:
Shrestha, B., X. Martini, and L.L. Stelinski. 2021. Population fluctuations of Diaphorina citri and its natural enemies in response to various management practices in Florida. Florida Entomologist. 104: 178-185.
- Type:
Journal Articles
Status:
Published
Year Published:
2021
Citation:
Killiny, N., Y. Nehela, J. George, M. Rashidi, L.L. Stelinski, S.L. Lapointe. 2021. Phytoene desaturase-silenced citrus as a trap crop with multiple cues to attract Diaphorina citri, the vector of Huanglongbing. Plant Science. 308: 110930.
- Type:
Journal Articles
Status:
Published
Year Published:
2021
Citation:
Gugliuzzo, A., P.H.W. Biedermann, D. Carrillo, L.A. Castrillo, J.P. Egonyu, D. Gallego, K. Haddi, J. Hulcr, H. Jactel, H. Kajimura, N. Kamata, N. Meurisse, Y. Li, J.B. Oliver, C.M. Ranger, D. Rassati, L.L. Stelinski, R. Sutherland, G. T. Garzia, M.G. Wright, and A. Biondi. 2021. Recent advances toward the sustainable management of invasive Xylosandrus ambrosia beetles. Journal of Pest Science. 94: 615-637.
- Type:
Journal Articles
Status:
Published
Year Published:
2021
Citation:
Chen, X.D., S. Neupane, H. Gossett, T.A. Ebert, H. Gossett, K. S. Pelz-Stelinski, and L.L. Stelinski. 2021. Insecticide rotation scheme restores insecticide susceptibility in thiamethoxam-resistant field populations of Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Leviidae) in Florida. Pest Management Science. 77: 464-473.
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Progress 11/21/19 to 09/30/20
Outputs
Target Audience:Citrus growers, productions managers, and agrochemical industry related to citriculture. Changes/Problems:None. What opportunities for training and professional development has the project provided?This project has trained 5 post-docs and 4 students. Two post-docs have recently graduated the prpgram.Justin George obtained a GS-13 Research Entomologist position with ARS in Mississippi and Freddy Ibanez began as an assistant professor of plant vector entomology at Texas A&M. How have the results been disseminated to communities of interest?The results have been disseminated though peer reviewed publications, extension publications in population magazines and university-sponsored extension publications. The results were also disseminated through presentations given at grower meetings and workshops. The results have also been disseminated using the internet via the Science for Citrus Health website. What do you plan to do during the next reporting period to accomplish the goals?My 2021 research program will focus on meeting the goals of existing USDA-APHIS-MAC and CRDF funding obtained prior to 2020, as well as, the newly obtained funding from USDA-SCRI-CDRE. My intention is to also continue to garner new funding for the lab. Specific areas of current research: Title: Why spray if you don't need to? Putting the IPM back into citrus IPM by ground truthing spray thresholds. Source: CRDF. Purpose: Implement injury thresholds to determine for need for insecticide applications for ACP. Title: Evaluation of a novel device for releasing volatile repellents against Asian citrus psyllid: optimizing active ingredient and deployment strategies for field-scale use. Source: USDA-APHIS-MAC. Purpose: Continue development of repellent device as a tool for ACP population suppression. Title: Field implementation of an advanced multimodal attract-and-kill device (CAPUT trap) for sustainable management of Asian citrus psyllid. Source: USDA-APHIS-MAC. Purpose: Continue development of attract-&-kill device as a tool for ACP population suppression. Title: Optimal Bt toxins and gene silencing RNAs for management of Asian citrus psyllid to mitigate impact of citrus greening. Source: USDA-NIFA. Purpose: Develop engineered citrus expressing Bt toxin for management of ACP. Combine with RNAi to mitigate resistance development and increase efficacy.
Impacts
What was accomplished under these goals?
My research program in 2020 focused primarily on insect and pathogen interactions and pest management in citrus and avocado. We made progress on several fundamental ecology projects; however, most of my research was geared toward practical application. I provide some in depth examples below. A large multi-grant and multi-state project my lab has been coordinating is development of an attract-&-kill device for ACP. This project is coming to its natural end. During the project, we developed two prototypes of a multimodal attract-and-kill device that is three dimensional in shape and includes elements of color, attractant, phagostimulant, UV reflectant and toxicant. All of these cues were optimized individually and then brought together for this device. Ingredients that were identified during the project were incorporated into a yellow slow-release wax (SPLAT) matrix and applied directly on the surface of a yellow cylinder or applied to corrugated plastic card and inserted inside a perforated cylinder. Psyllids landing on the device attempted to feed from the wax matrix, became intoxicated, died and fell from the device. Our laboratory and field experiments showed that the device attracted and killed significantly more adult ACP than ordinary yellow sticky cards and remained fully active over a period of 12 weeks. We have been in conversations with ISCA Technologies regarding commercialization of a product for field use. In avocado, my lab assessed the repellency of methyl salicylate and verbenone to two putative laurel wilt vectors in avocado,Xyleborus volvulusandXyleborus bispinatus, under laboratory conditions. Then, we tested the two chemicals released from SPLAT® with and without low-dose ethanol dispensers for manipulation of ambrosia beetle populations occurring in commercial avocado. The potential active space of repellents was assessed by quantifying beetle catch on traps placed 'close' (~ 5-10 cm) and 'far' (~ 1-1.5 m) away from repellent dispensers. Scolytidid beetle catch was reduced in the field more when plots were treated with verbenone dispensers co-deployed with low-dose ethanol dispensers than when treated with verbenone alone. Beetle diversity was highest near traps in plots where low-dose ethanol lures were deployed. The repellent treatments and ethanol lures significantly altered the species composition of beetles captured in experiment plots. Our results indicate that verbenone co-deployed with ethanol lures holds potential for manipulating ambrosia beetle vectors via push-pull management in avocado. We continue our work on resistance management of ACP, although this project is also slowly winding down. We demonstrated that ACP populations develop high levels of resistance to several of the main modes of action used for their management under continuous selection by label rate applications in cultivated citrus. For example, a high level of resistance occurs following only 3-4 consecutive neonicotinoid sprays and within five egg to adult generations and was associated with subsequent product failure. We also showed that resistance in ACP to declined significantly in the absence of selection pressure under laboratory conditions and when modes of action rotation was implemented after initially selecting for resistance under field conditions. Recovery to a susceptible state under rotation in the field was more rapid than under no selection in the laboratory population. These results suggest that resistance is likely unstable under the field conditions. We proved resistance to several modes of action caries significant fitness consequences in ACP. In effect, our results indicate that careful rotation solves the problem entirely. In my opinion, it would be useful to continue to monitor for resistance as long as insecticides are being used for ACP, because other mechanisms of resistance that are not apparent yet could evolve. Furthermore, failures of rotation occur for various reasons and it would be good to know if those are causing negative effects on ACP management. Consideration should be given regarding whether funding a monitoring program to maintain an up to date knowledge base of current susceptibility levels of ACP populations to insecticides in FL is worth the investment. We have also continued work on pathogen-plant-insect interactions, focusing on HLB. Citrus trees were exposed to either a 'one-time' 7-day Inoculation Access Period (IAP) or 'continuous' IAP for an entire year. We hypothesizeda priorithat those trees exposed to infected vectors for 7-day IAP (assuming 100% transmission) would continue to live and grow with lowCLas titer. In contrast, we expected those trees receiving constant re-inoculations fromCLas-infected ACP over the course of the experiment would develop highCLas titer and consequently succumb to the symptoms of HLB disease much faster. Astonishingly, we observed no difference inCLas titer between plants exposed to infected vectors for 7-day IAP, as compared with plants exposed continuously to a breeding population ofCLas-infected vectors over the course of an entire year of plant infection. Also, the presence/absence of the genomicCLas DNA in mature leaves was associated with intense periods of vegetative flush growth, suggesting that theCLas bacterium is transported through phloem during annual movement of carbon and nitrogen compounds needed for vegetative growth, including transportation from roots to mature leaves. We recently examined the mechanism(s) of immune response inC. sinensisvia accumulation of SA and its metabolites after prolonged feeding by uninfected ACP and determined that herbivory differentially regulated transcription and SA-metabolite accumulation in citrus leaves, depending on duration of insect feeding (Ibanez and Stelinski, 2020; Ibanez et al., 2019). Our results showed a significant upregulation ofBSMT-likeand concurrent downregulation of a methylesterase,MES1-like,in plants that had been exposed to ACP feeding for 150 d. Expression ofBSMT-likewas associated with an increase in methyl salicylate accumulation in mature leaves. Similarly, this outcome was observed for the expression profile ofDMR6-likeand accumulation of 2,3-DHBA (hydroxylated SA metabolite). Therefore, prolonged and uninterrupted exposure of citrus to ACP feeding modulates SA and accumulation of its metabolites in sweet orange. We hypothesized that a threshold [SA] exists inC. sinensisthat modulates the transcriptional regulation of genes involved in immune defenses and that the abnormal level of gene expression and metabolite accumulation under this scenario does not allow the host plant,C. sinensis, to mount a proper immune response (Ibanez et al., 2019). Based on this work, we submitted a proposal to USDA-SCRI-CDRE to elucidate the biological function of a set of genes associated with synthesis of SA and its metabolites and determine how its accumulation in plant tissues modulates SA-dependent immune responses to the pathogen and vector. The long-term goal of this project is to manipulate response ofCitrusto the vector-pathogen interaction to boost host plant defense response against HLB. Unfortunately, the reviewers did not agree that this apporach was critical to solving the HLB problem.
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2020
Citation:
George, J., S.L. Lapointe, L.T. Markle, J.M. Patt, S.A. Allan, M. Setamou, M.J. Rivera, J.A. Qureshi, and L.L. Stelinski. 2020. A multimodal attract-and-kill device for Asian citrus psyllid Diaphorina citri (Hemiptera: Liviidae). Insects. 11,870; https://doi.org/10.3390/insects11120870
- Type:
Journal Articles
Status:
Published
Year Published:
2020
Citation:
Martini, X., A. Hoyte, A. Mafra-Neto, A.A. Aksenov, C.E. Davis, and L.L. Stelinski. 2020. Progress toward an attract-and-kill device for Asian citrus psyllid (Hemiptera: Liviidae) using volatile signatures of citrus infected with huanglongbing as the attractant. Journal of Insect Science. 20(6): 25; 1-10. https://doi.org/10.1093/jisesa/ieaa126
- Type:
Journal Articles
Status:
Published
Year Published:
2020
Citation:
El-Desouky, A., J. George, K. Sturgeon, L.L. Stelinski, and R.G. Shatters. 2020. Asian citrus psyllid adults inoculate huanglongbing bacterium more efficiently than nymphs when this bacterium is acquired by early instar nymphs. Scientific Reports. 10: 18244. https://doi.org/10.1038/s41598-020-75249-5.
- Type:
Journal Articles
Status:
Published
Year Published:
2020
Citation:
Chen, X.D., M. Seo, T.A. Ebert, M. Ashfaq, W. Qin, and L.L. Stelinski. 2020. Hormesis in the brown citrus aphid, Toxoptera citricida (Kirkaldy) (Hemiptera: Aphididae) exposed to sublethal doses of imidacloprid. Florida Entomologist. 103: 337-343.
- Type:
Journal Articles
Status:
Published
Year Published:
2020
Citation:
Allan, S.A., J. George, L.L. Stelinski, and S.L. Lapointe. 2020. Attributes of yellow traps affecting attraction of Diaphorina citri (Hemiptera: Liviidae). Insects. 11, 452. https://doi.org/10.3390/insects11070452.
- Type:
Journal Articles
Status:
Published
Year Published:
2020
Citation:
Chen, X.D., T.A. Ebert, K.S. Pelz-Stelinski, and L.L. Stelinski. 2020. Fitness costs associated with thiamethoxam and imidacloprid resistance in three field populations of Diaphorina citri (Hemiptera: Liviidae) from Florida. Bulletin of Entomological Research. 110: 512-520.
- Type:
Journal Articles
Status:
Published
Year Published:
2020
Citation:
Martini, X., K. Malfa, L.L. Stelinski, F.B. Iriarte, and M.L. Paret. 2020. Distribution, phenology, and overwintering survival of Asian citrus psyllid in urban and grove habitats in North Florida. Journal of Economic Entomology. 113: 1080-1087.
- Type:
Journal Articles
Status:
Published
Year Published:
2020
Citation:
Liu, S-H., Y-D. Xia, Q. Zhang, W. Li, R-Y. Li, Y. Liu, E-H. Chen, W. Du, L.L. Stelinski, and J-J. Wang. 2020. Potential targets for controlling Bactrocera dorsalis using cuticle- and hormone-related genes revealed by a developmental transcriptome analysis. Pest Management Science. 76: 2127-2143.
- Type:
Journal Articles
Status:
Published
Year Published:
2020
Citation:
Ibanez F, L.L. Stelinski. 2020. Temporal dynamics of Candidatus Liberibacter asiaticus titer in mature leaves from Citrus sinensis cv Valencia are associated with vegetative growth. Journal of Economic Entomology. 113: 589-595.
- Type:
Journal Articles
Status:
Published
Year Published:
2020
Citation:
Rivera, M.J., X. Martini, D. Conover, A. Mafra-Neto, D. Carrillo, and L.L. Stelinski. 2020. Evaluation of semiochemical based push-pull strategy for population suppression of ambrosia beetle pathogen vectors in avocado. Scientific Reports. 10: 2670; https://doi.org/10.1038/s41598-020-59569-0.
- Type:
Journal Articles
Status:
Published
Year Published:
2020
Citation:
George, J., T.M. Paris, S.D. Allan, S.L. Lapointe, and L.L. Stelinski. 2020. UV reflective properties of magnesium oxide increase attraction and probing behavior of Asian citrus psyllids (Hemiptera: Liviidae). Scientific Reports. 10: 1890; https://doi.org/10.1038/s41598-020-58593-4.
- Type:
Journal Articles
Status:
Published
Year Published:
2020
Citation:
Hassani-Kakhki, M., N. Karimi, F. El Borai, N. Killiny, M. Hosseini, L.L. Stelinski, and L. Duncan. 2020. Drought stress impairs communication between potato (Solanum tuberosum) and subterranean biological control agents. Annals of the Entomological Society of America. 113: 23-29.
- Type:
Journal Articles
Status:
Published
Year Published:
2020
Citation:
George, J., R. Kanissery, E.-D. Ammar, I. Cabral, L.T. Markle, J.M. Patt, and L.L. Stelinski. 2020. Feeding behavior of Asian citrus psyllid [Diaphorina citri (Hemiptera: Liviidae)] nymphs and adults on common weeds occurring in cultivated citrus described using electrical penetration graph recordings. Insects. 11, 48; https://doi.org/10.3390/Insects11010048.
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