Keywords
vector control
electropenetography
citrus
Asian citrus psyllid
Categories
How to Cite
Abstract
Protecting plants by targeting insect vectors of pathogenic organisms requires an intimate understanding of the biology of the insect, the pathogen, and the plant host at a spatial scale relevant to the insect. Observing insect feeding is difficult because insect mouthparts are small, and many insects insert their mouthparts deep inside plants, where we cannot see them. Electropenetrography (EPG) is the only technique that overcomes these problems. Using EPG, we can understand host-insect relationships, pesticide action, and the role of non-hosts. EPG can address ecological questions like "how do insects survive long migrations over regions devoid of known host plants?" It can also address applied questions: "will the pest feed on my new cultivar?" This light introduction to an underused key technology focuses on the Asian citrus psyllid, but EPG has great potential to improve pest management efforts for several different crops and insect vectors.
References
AES. 2024. Insect Mouthparts. https://www.amentsoc.org/insects/fact-files/mouthparts.html
Ammar, E.-D., D. G. Hall, and R. G. Shatters, Jr. 2013. “Stylet Morphometrics and Citrus Leaf Vein Structure in Relation to Feeding Behavior of the Asian Citrus Psyllid Diaphorina citri, Vector of Citrus Huanglongbing Bacterium.” Plos One. https://doi.org/10.1371/journal.pone.0059914
Backus, E. A., and H. T. Shih. 2020. “Review of the EPG Waveforms of Sharpshooters and Spittlebugs Including Their Biological Meanings in Relation to Transmission of Xylella fastidiosa (Xanthomonadales: Xanthomonadaceae).” Journal of Insect Science 20(4). https://doi.org/10.1093/jisesa/ieaa055
Brasier, C. M. 2001. “Rapid Evolution of Introduced Plant Pathogens via Interspecific Hybridization.” Bioscience 51:123–133. https://doi.org/10.1641/0006-3568(2001)051[0123:REOIPP]2.0.CO;2
CDC. 2020. Vaccine administration: Needle gauge and length. https://www.cdc.gov/vaccines/hcp/admin/downloads/vaccine-administration-needle-length.pdf
CDFA. 2024. Asian citrus psyllid host list. https://www.cdfa.ca.gov/plant/pdep/target_pest_disease_profiles/hostlists/AsianCitrusPsyllid-HostList.pdf
Cervantes, F. A., and E. A. Backus. 2015. “Amount of Applied Signal Voltage Affects Behaviors in EPG Recordings of Lygus lineolaris Adults on Pinhead Cotton Squares.” Annual Meeting of the Entomological Society of America. Entomological Society of America, Minneapolis, MN. Nov 2015.
Cervantes, F. A., and E. A. Backus. 2018. “EPG Waveform Library for Graphocephala atropunctata (Hemiptera: Cicadellidae): Effect of Adhesive, Input Resistor, And Voltage Levels on Waveform Appearance and Stylet Probing Behaviors.” Journal of Insect Physiology 109:21–40. https://doi.org/10.1016/j.jinsphys.2018.05.008
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: Aphididiae) Exposed to Sublethal Doses of Imidacloprid.” Florida Entomologist 103: 337–343. https://doi.org/10.1653/024.103.0305
Chernova, T. E., P. V. Mikshina, V. V. Salnikov, N. N. Ibragimova, O. V. Sautkina, and T. A. Gorshkova. 2018. “Development of Distinct Cell Wall Layers Both in Primary and Secondary Phloem Fibers of Hemp (Cannabis sativa L.).” Industrial Crops and Products 117: 97–109. https://doi.org/10.1016/j.indcrop.2018.02.082
Chesnais, Q., and K. E. Mauck. 2018. “Choice of Tethering Material Influences the Magnitude and Significance of Treatment Effects in Whitefly Electrical Penetration Graph Recordings.” Journal of Insect Behavior 31:656–671. https://doi.org/10.1007/s10905-018-9705-x
Cifuentes-Arenas, J. C., A. de Goes, M. P. de Miranda, G. A. C. Beattie, and S. A. Lopes. 2018b. “Citrus Flush Shoot Ontogeny Modulates Biotic Potential of Diaphorina citri.” Plos One 13:1–17. https://doi.org/10.1371/journal.pone.0190563
Cooper, W. R., D. R. Horton, M. R. Wildung, A. S. Jensen, J. Thinakaran, D. Rendon, L. B. Nottingham, et al. 2019. “Host and Non-Host 'Whistle Stops' for Psyllids: Molecular Gut Content Analysis by High-Throughput Sequencing Reveals Landscape-Level Movements of Psylloidea (Hemiptera).” Environmental Entomology 48:554–566. https://doi.org/10.1093/ee/nvz038
Cutler, G. C., M. Amichot, G. Benelli, R. N. C. Guedes, Y. Qu, R. R. Rix, F. Ullah, and N. Desneux. 2022. “Hormesis and Insects: Effects and Interactions in Agroecosystems.” Science of the Total Environment 825:153899. https://doi.org/10.1016/j.scitotenv.2022.153899
Ebert, T. A., and M. E. Rogers. 2016. “Effect of Substrate Voltage on EPG Recordings of Ingestion and Probing Behavior in Diaphorina citri (Hemiptera: Liviidae).” Florida Entomologist 99:528–534. https://doi.org/10.1653/024.099.0328
Ebert, T. A., E. A. Backus, H. J. Shugart, and M. E. Rogers. 2018. “Behavioral Plasticity in Probing by Diaphorina citri (Hemiptera, Liviidae): Ingestion from Phloem versus Xylem Is Influenced by Leaf Age and Surface.” Journal of Insect Behavior 31:119–137. https://doi.org/10.1007/s10905-018- 9666-0
Ebert, T. A., E. Backus, M. Cid, A. Fereres, and M. Rogers. 2015. “A New SAS Program for Behavioral Analysis of Electrical Penetration Graph Data.” Computers and Electronics in Agriculture 116:80–87. https://doi.org/10.1016/j.compag.2015.06.011
Fancelli, M., M. Borges, R. A. Laumann, J. A. Pickett, M. A. Birkett, and M. C. Blassioli-Moraes. 2018. “Attractiveness of Host Plant Volatile Extracts to the Asian Citrus Psyllid, Diaphorina citri, is Reduced by Terpenoids from the Non-Host Cashew.” Journal of Chemical Ecology 44:397–405. https://doi.org/10.1007/s10886-018-0937-1
George, J., E. D. Ammar, D. G. Hall, R. G. Shatters, Jr., and S. L. Lapointe. 2018. “Prolonged Phloem Ingestion by Diaphorina citri Nymphs Compared to Adults Is Correlated with Increased Acquisition of Citrus Greening Pathogen.” Scientific Reports 8:10352. https://doi.org/10.1038/s41598-018-28442-6
George, J., R. Kanissery, M. Bashyal, B. Tamayo, and L. L. Stelinski. 2022. “Survival and Feeding Behavior of Diaphorina citri (Hemiptera: Liviidae) Adults on Common Cover Crops in Citrus.” Agriculture 12. https://doi.org/10.3390/agriculture12122175
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
Goss, E. M., M. E. Cardenas, K. Myers, G. A. Forbes, W. E. Fry, S. Restrepo, and N. J. Grunwald. 2011. “The Plant Pathogen Phytophthora andina Emerged via Hybridization of an Unknown Phytophthora Species and the Irish Potato Famine Pathogen, P. infestans.” Plos One 6:e24543. https://doi.org/10.1371/journal.pone.0024543
Guz, N., M. Arshad, N. S. Cagatay, A. Dageri, and M. I. Ullah. 2020. “Detection of Wolbachia (Rickettsiales: Anaplasmataceae) and Candidatus Liberibacter asiaticus (Rhizobiales: Rhizobiaceae) Associated with Diaphorina citri (Hemiptera: Liviidae) Collected from Citrus reticulata (Sapindales: Rutaceae) and Alternate Host, Cordia myxa (Boraginales: Boraginaceae).” Journal of Economic Entomology 113:1486–1492. https://doi.org/10.1093/jee/toaa043
Hijaz, F., and N. Killiny. 2014. “Collection and Chemical Composition of Phloem Sap from Citrus sinensis L. Osbeck (Sweet Orange).” Plos One 9:1–11. https://doi.org/10.1371/journal.pone.0101830
Hoffmann, G. R. 2009. “A Perspective on the Scientific, Philosophical, and Policy Dimensions of Hormesis.” Dose Response 7:1–51. https://doi.org/10.2203/dose-response.08-023.Hoffmann
Jiang, Y., C. X. Zhang, R. Chen, and S. Y. He. 2019. “Challenging Battles of Plants with Phloem-Feeding Insects and Prokaryotic Pathogens.” Proceedings of the National Academy of Science U S A 116: 23390–23397. https://doi.org/10.1073/pnas.1915396116
Kessler, A., and A. Kalske. 2018. “Plant Secondary Metabolite Diversity and Species Interactions.” Annual Review of Ecology, Evolution, and Systematics 49:115–138. https://doi.org/10.1146/annurev-ecolsys-110617-062406
Kim, K. D. 2013. “Integrated Management of Asian Citrus Psyllid, Diaphorina citri Kuwayama, for Protecting Young Citrus Trees from Huanglongbing.” PhD dissertation, University of Florida Gainesville, Florida. https://ufdcimages.uflib.ufl.edu/UF/E0/04/62/49/00001/KIM_K.pdf
Langdon, K. W., T. A. Ebert, and M. E. Rogers. 2019. “Evaluating the Effect of Imidacloprid Administered in Artificial Diet on Feeding Behavior of Diaphorina citri (Hemiptera: Liviidae) Using Electropenetrography.” Journal of Economic Entomology 112:644–652. https://doi.org/10.1093/jee/toy400
Lei, H., W. F. Tjallingii, and J. C. van Lenteren. 2009. “Effect of Tethering during EPG Recorded Probing by Adults of the Greenhouse Whitefly.” Journal of Applied Entomology 121:211–217. https://doi.org/10.1111/j.1439-0418.1997.tb01395.x
Lewis-Rosenblum, H., X. Martini, S. Tiwari, and L. L. Stelinski. 2015. “Seasonal Movement Patterns and Long-Range Dispersal of Asian Citrus Psyllid in Florida Citrus.” Journal of Economic Entomology 108:3–10. https://doi.org/10.1093/jee/tou008
Martini, X., A. Hoyte, and L. L. Stelinski. 2014. “Abdominal Color of the Asian Citrus Psyllid (Hemiptera: Liviidae) is Associated with Flight Capabilities.” Annals of the Entomological Society of America 107:842–847. https://doi.org/10.1603/AN14028
Nel, P., S. Bertrand, and A. Nel. 2018. “Diversification of Insects since the Devonian: A New Approach Based on Morphological Disparity of Mouthparts.” Scientific Reports 8:3516. https://doi.org/10.1038/s41598-018-21938-1
Pec, M., E. A. Ferreira, and M. Penaflor. 2023. “Association of Non-Host Crop Plants with Mandarin in Host Location and Survival of Diaphorina citri Kuwayama (Hemiptera: Psyllidae).” Neotropical Entomology 53:304–313. https://doi.org/10.1007/s13744-023-01107-4
Pelz-Stelinski, K. S., R. H. Brlansky, T. A. Ebert, and M. E. Rogers. 2010. “Transmission Parameters for Candidatus Liberibacter asiaticus by Asian Citrus Psyllid (Hemiptera: Psyllidae).” Journal of Economic Entomology 103:1531–1541. https://doi.org/10.1603/EC10123
Ramsey, J. S., E. D. Ammar, J. E. Mahoney, K. Rivera, R. Johnson, D. O. Igwe, T. W. Thannhauser, M. J. MacCoss, D. G. Hall, and M. Heck. 2022. “Host Plant Adaptation Drives Changes in Diaphorina citri Proteome Regulation, Proteoform Expression, and Transmission of ‘Candidatus Liberibacter asiaticus’, the Citrus Greening Pathogen.” Phytopathology. 112:101–115. https://doi.org/10.1094/PHYTO-06-21-0275-R
Ristaino, J. B., P. K. Anderson, D. P. Bebber, K. A. Brauman, N. J. Cunniffe, N. V. Fedoroff, C. Finegold, et al. 2021. “The Persistent Threat of Emerging Plant Disease Pandemics to Global Food Security.” Proceedings of the National Academy of Science U S A 118 (23): e2022239118. https://doi.org/10.1073/pnas.2022239118
Santos Silva, M., J. M. Patt, C. de Jesus Barbosa, M. Fancelli, P. Roberto Ribeiro Mesquita, F. de Medeiros Rodrigues, and A. Selbach Schnadelbach. 2023. “Asian Citrus Psyllid, Diaphorina citri (Hemiptera: Liviidae) Responses to Plant-Associated Volatile Organic Compounds: A Mini-Review.” Crop Protection 169:106242. https://doi.org/10.1016/j.cropro.2023.106242
Schultz, J. C., H. M. Appel, A. P. Ferrieri, and T. M. Arnold. 2013. “Flexible Resource Allocation during Plant Defense Responses.” Frontiers in Plant Science 4:324. https://doi.org/10.3389/fpls.2013.00324
Shugart, H. 2019. “Probing Behavior and Host Preference in the Asian Citrus Psyllid, Diaphorina citri (Hemiptera: Liviidae).” PhD dissertation, University of Florida Gainesville. https://original-ufdc.uflib.ufl.edu/UFE0054047/00001
Shugart, H., T. Ebert, F. Gmitter, and M. Rogers. 2019. “The Power of Electropenetrography in Enhancing Our Understanding of Host Plant-Vector Interactions.” Insects 10:1–22. https://doi.org/10.3390/insects10110407
Son, Y., E. A. Backus, R. L. Groves, and M. W. Johnson. 2012. “Pattern of Stylet Penetration Activity by Homalodisca vitripennis (Hemiptera: Cicadellidae) Adults in Relation to Environmental Temperature and Light Conditions.” Environmental Entomology 41:1215–1230. https://doi.org/10.1603/EN11319
Stelinski, L. L. 2019. “Ecological Aspects of the Vector-Borne Bacterial Disease, Citrus Greening (Huanglongbing): Dispersal and Host Use by Asian Citrus Psyllid, Diaphorina citri Kuwayama.” Insects 10:1–11. https://doi.org/10.3390/insects10070208
Tao, T., Z. Wang, R. Mao, M. Hussain, S. P. Arthurs, F. Ye, X. An, and J. Gao. 2023. “Vermicompost Amendments Disrupt Feeding Behavior of Diaphorina citri Kuwayama and Boost Activities of Salicylic Acid and Jasmonic Acid Pathway-Related Enzymes in Citrus.” Insects 14 (5): 410. https://doi.org/10.3390/insects14050410
Van Damme, W., R. Dahake, R. van de Pas, G. Vanham, and Y. Assefa. 2021. “COVID-19: Does the Infectious Inoculum Dose-Response Relationship Contribute to Understanding Heterogeneity in Disease Severity and Transmission Dynamics?” Medical Hypotheses 146:110431. https://doi.org/10.1016/j.mehy.2020.110431
Wang, L., J. Zhu, Q. Wang, X. Ji, W. Wang, W. Huang, C. Rui, and L. Cui. 2023. “Hormesis Effects of Sulfoxaflor on Aphis gossypii Feeding, Growth, Reproduction Behaviour and the Related Mechanisms.” Science of the Total Environment 872:162240. https://doi.org/10.1016/j.scitotenv.2023.162240
Zhang, R. M., S. Y. He, W. Wu, Y. J. Huang, C. Y. Zhu, F. Xiao, Z. Y. Liu, and J. W. Zeng. 2019. “Survival and Lifespan of Diaphorina citri on Non-Host Plants at Various Temperatures.” Crop Protection 124:104841. https://doi.org/10.1016/j.cropro.2019.06.001
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Copyright (c) 2025 UF/IFAS