Use and perspective of entomopathogenic fungi biocontrol agents of Asian citrus psyllid (Diaphorina citri): A bibliometric review
DOI:
https://doi.org/10.33448/rsd-v12i12.43984Keywords:
Entomopathogenic fungi; Diaphorina citri; Greening; Biological control; Bibliometric analysis.Abstract
The Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), is the main insect vector of the bacteria Candidatus liberibacter spp., which are the causative agents of Citrus Greening disease, also known as Huanglongbing (HLB). The current lack of treatment for the disease means that intensive work is required to manage psyllid populations, mainly through chemical control methods. Since biological control has become a promising management strategy and entomopathogenic fungi are one of the components of integrated pest management, this review aimed to compare previously published results regarding the most efficient fungi for controlling D. citri and to gather information about the best options available. To this end, the bibliography indexed in the Scopus and Web of Science databases was analyzed using bibliometric tools with the R Studio software and the Bibliometrix package. In recent years, Cordyceps fumosorosea, Beauveria bassiana, and Hirsutella citriformis were identified as the most relevant fungus species, showing efficient results. In addition, the countries that publish the most on this subject are also among the largest citrus producers. Studies performed under greenhouse and field conditions are still scarce but necessary to validate the results obtained in the laboratory, as well as those that explore the mechanisms of action involved in the pathogenicity of fungi against D. citri, which are matters to consider in future assessments.
References
Aguila, L. C. R., Akutse, K. S., Ashraf, H. J., Bamisile, B. S., Lin, J., Dai, J., Wang, H., & Wang, L. (2021). The survival and parasitism rate of Tamarixia radiata (Hymenoptera: Eulophidae) on its host exposed to Beauveria bassiana (Ascomycota: Hypocreales). Agronomy, 11 (8), 1496.
Aguila, L. C. R., Ashraf, H. J., Moreano, J. P. S., Akutse, K. S., Bamisile, B. S., Lu, L., Li, X., Lin, J., Wu, Q., & Wang, L. (2022). Genome-wide identification and characterization of toll-like receptors (TLRs) in Diaphorina citri and their expression patterns induced by the endophyte Beauveria bassiana. Journal of Fungi, 8, 888.
Allaire, J. (2012). RStudio: integrated development environment for R. Boston, MA, 770 (394), 165–171.
Aria, M., & Cuccurullo, C. (2017). bibliometrix: An R-tool for comprehensive science mapping analysis. Journal of informetrics, 11 (4), 959–975.
Arnosti, A., Junior, I. D., Conceschi, M. R., D’Alessandro, C. P., Travaglini, R. V., & Camargo-Mathias, M. I. (2019). Interactions of adjuvants on adhesion and germination of Isaria fumosorosea on adults of Diaphorina citri. Scientia Agricola, 76 (6), 487–493.
Ausique, J. J. S., D’Alessandro, C. P., Conceschi, M. R., Mascarin, G. M., & Delalibera Júnior, I. (2017). Efficacy of entomopathogenic fungi against adult Diaphorina citri from laboratory to field applications. Journal of Pest Science, 90 (3), 947-960.
Avery, P. B., Duren, E. B., Qureshi, J. A., Adair, R. C. J., Adair, M. M., & Cave, R. D. (2021). Field efficacy of Cordyceps javanica, white oil and spinetoram for the management of the Asian citrus psyllid, Diaphorina citri. Insects, 12 (9), 824.
Avery, P. B., Pick, D. A., Aristizábal, L. F., Kerrigan, J., Powell, C. A., Rogers, M. E., & Arthurs, S. P. (2013). Compatibility of Isaria fumosorosea (Hypocreales: Cordycipitaceae) blastospores with agricultural chemicals used for management of the Asian citrus psyllid, Diaphorina citri (Hemiptera: Liviidae). Insects, 4, 694-711.
Awan, U. A., Meng, L., Xia, S., Raza, M. F., Zhang, Z., & Zhang, H. (2021a) Isolation, fermentation, and formulation of entomopathogenic fungi virulent against adults of Diaphorina citri. Pest Management Science, 77 (9), 4040–4053.
Awan, U. A., Xia, S., Meng, L., Raza, M. F., Zhang, Z., & Zhang, H. (2021b). Isolation, characterization, culturing, and formulation of a new Beauveria bassiana fungus against Diaphorina citri. Biological Control, 158.
Bamisile, B. S., Dash, C. K., Akutse, K. S., Qasim, M., Aguila, L. C. R., Wang, F., Keppanan, R., & Wang, L. (2019). Endophytic Beauveria bassiana in foliar-treated Citrus limon plants acting as a growth suppressor to three successive generations of Diaphorina citri Kuwayama (Hemiptera: Liviidae). Insects, 10 (6), 176.
Bové, J. M. (2014). Huanglongbing or yellow shoot, a disease of Gondwanan origin: will it destroy citrus worldwide? Phytoparasitica, 42, 579–583.
Chen, X. D., Gill, T. A., Ashfaq, M., Pelz-Stelinski, K. S., & Stelinski, L. L. (2018). Resistance to commonly used insecticides in Asian citrus psyllid: Stability and relationship to gene expression. Journal of Applied Entomology, 142 (10), 967–977.
Chow, A., Dunlap, C. A., Jackson, M. A., Flores, D., Patt, J. M., & Sétamou, M. (2016). Oviposition behavior and survival of Tamarixia radiata (Hymenoptera: Eulophidae), an ectoparasitoid of the Asian citrus psyllid, Diaphorina citri (Hemiptera: Liviidae), on hosts exposed to an entomopathogenic fungus, Isaria fumosorosea (Hypocreales: Cordycipitaceae), under laboratory conditions. Journal of Economic Entomology, 109 (5), 1995–2005.
Chow, A., Dunlap, C. A., Jackson, M. A., Avery, P. B., Patt, J. M., & Sétamou, M. (2018). Field efficacy of autodissemination and foliar sprays of an entomopathogenic fungus, Isaria fumosorosea (Hypocreales: Cordycipitaceae), for control of Asian citrus psyllid, Diaphorina citri (Hemiptera: Liviidae), on residential citrus. Journal of Economic Entomology, 111 (5), 2089–2100.
Cisneros, J., Wendel, J., Jaronski, S., Vitek, C., Ciomperlik, M., & Flores, D. (2022). Assessment of Two Novel Host-Derived Beauveria bassiana (Hypocreales: Cordycipitaceae) Isolates Against the Citrus Pest, Diaphorina citri (Hemiptera: Liviidae). Journal of Economic Entomology, 115 (1), 56-64.
Conceschi, M. R., D’Alessandro, C. P., Moral, R. A., Demétrio, C. G. B., & Júnior, I. D. (2016). Transmission potential of the entomopathogenic fungi Isaria fumosorosea and Beauveria bassiana from sporulated cadavers of Diaphorina citri and Toxoptera citricida to uninfected D. citri adults. BioControl, 61 (5), 567–577.
Corrêa, B., Duarte, V. S., Silva, D. M., Mascarin, G. M., & Júnior, I. D. (2020). Comparative analysis of blastospore production and virulence of Beauveria bassiana and Cordyceps fumosorosea against soybean pests. BioControl, 65 (3), 323–337.
Cortez-Madrigal, H., Sánchez-Saavedra, J. M.,Díaz-Godínez, G., & Mora-Aguilera, G. (2014). Enzymatic activity and pathogenicity of entomopathogenic fungi from central and southeastern Mexico to Diaphorina citri (Hemiptera: Psyllidae). Southwestern Entomologist, 39 (3), 491-502.
Costa Lima, A. M. (1942). Insetos do Brasil, Homoptera. Rio de Janeiro: Escola Nacional de Agronomia, 3, 327 pp.
Cruz-Cruz, D., Gómez-Ruiz, J., Barrera, J. F., Sánchez-Peña, S. R., & Mora, J. F. V. (2020). Pathogenicity of Beauveria bassiana against immature stages of Diaphorina citri under laboratory conditions. Southwestern Entomologist, 45 (3), 609-620.
Cruz-Juárez, G., Maldonado-Blanco, M. G., Rodríguez-Guerra, R., Torre-Zavala, S., Avilés-Arnaut, H., & Flores-González, M. S. (2018). Mutation to increase sporulation of a strain of Hirsutella citriformis from Mexico and evaluation against Diaphorina citri. Southwestern Entomologist, 43 (4), 891-904.
Derviş, H. (2019). Bibliometric analysis using Bibliometrix an R Package. Journal of Scientometric Research, 8 (3), 156–160.
Gandarilla-Pacheco, F. L., López-Arroyo, J. I., Galán-Wong, L. J., & Quintero-Zapata, I. (2013). Patogenicity of native entomopathogenic fungi from the Mexican citrus-growing area against Diaphorina citri Kuwayama (Hemiptera: Liviidae). Southwestern Entomologist, 38 (2), 325-338.
González, O. P., Flores, R. G., & Guerra, P. T. (2022). Insight into biological control potential of Hirsutella citriformis against Asian citrus psyllid as a vector of citrus huanglongbing disease in America. Journal of Fungi, 8 (6), 573.
Hussain, M., Avery, P.B., Zhu, W., Pitino, M., Arthurs, S.P., Wang, L., Qiu, D., & Mao, R. (2021). Pathogenicity of Cordyceps javanica (Hypocreales: Cordycipitaceae) to Diaphorina citri (Hemiptera: Liviidae) adults, with ultrastructural observations on the fungal infection process. Agronomy, 11, 2476.
Ibarra-Cortés, K. H., González-Hernández, H., & Guzmán-Franco, A. W. (2017). Susceptibility of nymphs and adults of Diaphorina citri to the entomophathogenic fungus Hirsutella citriformis. Biocontrol Science and Technology, 27 (3), 433-438.
Ibarra-Cortés, K. H., González-Hernández, H., Guzmán-Franco, A. W., Ortega-Arenas, L. D., Villanueva-Jiménez, J. A., & Robles-Bermúdez, A. (2017). Interactions between entomopathogenic fungi and Tamarixia radiata (Hymenoptera: Eulophidae) in Diaphorina citri (Hemiptera: Liviidae) populations under laboratory conditions. Journal of Pest Science, 91 (1), 373–384.
Jalal, S. K. (2019). Co-authorship and co-occurrences analysis using Bibliometrix R-package: a casestudy of India and Bangladesh. Annals of Library and Information Studies (ALIS), 66 (2), 57–64.
Keppanan, R., Krutmuang, P., Sivaperumal, S., Hussain, M., Bamisile, B. S., Aguila, L. C. R., Dash, C. K., & Wang, L. (2018). Synthesis of mycotoxin protein IF8 by the entomopathogenic fungus Isaria fumosorosea and its toxic effect against adult Diaphorina citri. International Journal of Biological Macromolecules, 125, 1203–1211.
Keppanan, R., Sivaperumal, S., Hussain, M., Bamisile, B. S., Aguila, L. C. R., Qasim, M., Mekchay, S., Wang, L., & Krutmuang, P. (2019). Molecular characterization of pathogenesis involving the GAS 1 gene from entomopathogenic fungus Lecanicillium lecanii and its virulence against the insect host Diaphorina citri. Pesticide Biochemistry and Physiology, 157, 99–107.
Kumar, V., Avery, P., Ahmed, J., Cave, R., McKenzie, C., & Osborne, L. (2017). Compatibility and efficacy of Isaria fumosorosea with horticultural oils for mitigation of the Asian citrus psyllid, Diaphorina citri (Hemiptera: Liviidae). Insects, 8 (4), 119.
Lu, L., Cheng, B., Du, D., Hu, X., Peng, A., Pu, Z., Zhang, X., Huang, Z., & Chen, G. (2015). Morphological, molecular and virulence characterization of three Lencanicillium species infecting Asian citrus psyllids in Huangyan citrus groves. Journal of Invertebrate Pathology, 125, 45–55.
Luo, Y. Wu, S., He, X., Wang, D., He, Y., & Nian, X. (2022). Identification of a Cordyceps fumosorosea fungus isolate and its pathogenicity against Asian Citrus Psyllid, Diaphorina citri (Hemiptera: Liviidae). Insects, 13 (4), 374.
Maluta, N., Castro, T., & Lopes, J. R. S. (2022). Entomopathogenic fungus disrupts the phloem-probing behavior of Diaphorina citri and may be an important biological control tool in citrus. Scientific Reports, 12, 7959.
Mead, F. W., & Fasulo, T. R. (2011). Asian citrus psyllid, Diaphorina citri Kuwayama (Insecta: Hemiptera: Psillidae). Entomology and Nematology Department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida. Document no. EENY-033, 8 pp.
Mellín-Rosas, M. A., Sánchez-González, J. A., Cruz-Ávalos, A. M., Montesinos-Matías, R., & Arredondo-Bernal, H. C. (2016). Patogenicidad de cepas de hongos entomopatógenos sobre Diaphorina citri Kuwayama en condiciones de laboratório. Southwestern Entomologist, 41 (3), 791-800.
Morales-Reyes, C., Mascarin, G. M., Jackson, M. A., Hall, D., Sánchez-Peña, S. R., & Arthurs, S. P. (2018). Comparison of aerial conidia and blastospores from two entomopathogenic fungi against Diaphorina citri (Hemiptera: Liviidae) under laboratory and greenhouse conditions. Biocontrol Science and Technology, 28 (8), 737-749.
Orduño-Cruz, N., Guzmán-Franco, A. W., & Rodríguez-Leyva, E. (2015). Diaphorina citri populations carrying the bacterial plant pathogen Candidatus Liberibacter asiaticus are more susceptible to infection by entomopathogenic fungi than bacteria-free populations. Agricultural and Forest Entomology, 18 (1), 95–98.
Orduño-Cruz, N., Guzmán-Franco, A. W., Rodríguez-Leyva, E., Alatorre-Rosas, R., González-Hernández, H., Mora-Aguilera, G., & Rodríguez-Maciel, J. C. (2015a). In vitro selection of a fungal pathogen for use against Diaphorina citri. Biological Control, 90, 1-6.
Orduño-Cruz, N., Guzmán-Franco, A. W., Rodríguez-Leyva, E., Alatorre-Rosas, R., González-Hernández, H., & Mora-Aguilera, G. (2015b). In vivo selection of entomopathogenic fungal isolates for control of Diaphorina citri (Hemiptera: Liviidae). Biological Control, 90, 1-5.
Ou, D., Zhang, L. H., Guo, C. F., Chen, X. S., Ali, S., & Qiu, B. L. (2019). Identification of a new Cordyceps javanica fungus isolate and its toxicity evaluation against Asian citrus psyllid. MicrobiologyOpen, 8 (6).
Patt, J. M., Chow, A., Meikle, W. G., Gracia, C., Jackson, M. A., Flores, D., Sétamou, M., Dunlap, C. A., Avery, P. B., Hunter, W. B., & Adamczyk, J. J. (2015). Efficacy of an autodisseminator of an entomopathogenic fungus, Isaria fumosorosea, to suppress Asian citrus psyllid, Diaphorina citri, under greenhouse conditions. Biological Control, 88, 37–45.
Pérez-González, O., Arredondo-Bernal, H. C., Montesinos-Matías, R., Mellín-Rosas, M. A., & Maldonado-Blanco, M. G. (2020). Effect of native strains of Hirsutella citriformis on Diaphorina citri adults under field conditions. Southwestern Entomologist, 45 (2), 435-444.
Pérez-González, O., Gomez-Flores, R., & Tamez-Guerra, P. (2022). Insight into biological control potential of Hirsutella citriformis against Asian citrus psyllid as a vector of citrus huanglongbing disease in America. Journal of Fungi, 8 (6), 573.
Pérez-González, O., Maldonado-Blanco, M. G., & Valdes-Gonzalez, A. (2019). Conidia shelf-life and pathogenicity of strains of Hirsutella citriformis Speare against Diaphorina citri Kywayama produced on rice. Southwestern Entomologist, 44 (1), 165-171.
Pérez-González, O., Sandoval-Coronado, C. F., & Maldonado-Blanco, M. G. (2016). Evaluation of Mexican strains of Hirsutella citriformis against Diaphorina citri in a semifield bioassay. Southwestern Entomologist, 41 (2), 361-372.
Pérez-González, O., Rodríguez-Guerra, R., López-Arroyo, J. I., Sandoval-Coronado, C. F., &Maldonado-Blanco, M. G. (2015). Radial growth, sporulation, and virulence of Mexican isolates of Hirsutella citriformis against Diaphorina citri. Southwestern Entomologist, 40 (1), 111-120.
Pick, D. A., Avery, P. B., Qureshi, J. A., Arthurs, S. P., & Powell, C. A. (2022). Field persistence and pathogenicity of Cordyceps fumosorosea for management of Diaphorina citri. Biocontrol Science and Technology, 32 (2), 151-162.
Qasim, M., Xiao, H., He, K., Omar, M. A. A., Hussain, D., Noman, A., Rizwan, M., Khan, K. A., Al-zoubi, O. M., Alharbi, S. A., Wang, L., & Li, F. (2021). Host-pathogen interaction between Asian citrus psyllid and entomopathogenic fungus (Cordyceps fumosorosea) is regulated by modulations in gene expression, enzymatic activity and HLB-bacterial population of the host. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 248.
Quiroz, R. c., Maldonado, J. J. c., Alanis, M. J. R., Torres, J. A., & Saldívar, R. P. (2019). Fungi-based biopesticides: shelf-life preservation technologies used in commercial products. Journal of Pest Science, 92, 1003–1015.
Rosas-García, N. M., Alba-Moreno, I. M., Villegas-Mendoza, J. M., & Mireles-Martínez, M. (2018a). Biological activity of Metarhizium anisopliae strains and essential oils alone and in combination against Diaphorina citri. Southwestern Entomologist, 43 (3), 617-624.
Rosas-García, N. M., López-Barrera, G. L., Mireles-Martínez, M., & Villegas-Mendoza, J. M. (2018b). Activación de las isoformas del gen Pr1 de Metarhizium anisopliae durante la patogénesis en Diaphorina citri. Southwestern Entomologist, 43 (1), 199-207.
USDA – United States Department of Agriculture. (2023). Citrus: World Markets and Trade. https://www.fas.usda.gov/data/citrus-world-markets-and-trade
Vanaclocha, P., Jones, M. M., Tansey, J. A., Monzo, C., Chen, X. L., & Stansly, P. A. (2019). Residual toxicity of insecticides used against the Asian citrus psyllid and resistance management strategies with thiamethoxam and abamectin. Journal of Pest Science, 92 (2), 871–883.
Wei, G., Lai, Y. L., Wang, G. D., Chen, H., Li, F., & Wang, S. B. (2017). Insect pathogenic fungus interacts with the gut microbiota to accelerate mosquito mortality. Proceedings of the National Academy of Science, 114, 5994–5999.
Wendel, J., Cisneros, J., Jaronski, S., Vitek, C., Ciomperlik, M., & Flores, D. (2022). Screening commercial entomopathogenic fungi for the management of Diaphorina citri populations in the Lower Rio Grande Valley, Texas, USA. BioControl, 67, 225–235.
Yan, J., Liu, H., Idrees, A., Chen, F., Lu, H., Ouyang, G., & Meng, X. (2022). First record of Aspergillus fijiensis as an entomopathogenic fungus against Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae). Journal of Fungi, 8 (11), 1222.
Yang, Z., Wu, Q., Fan, J., Huang, J., Wu, Z., Lin, J., Bin, S., & Shu, B. (2021). Effects of the entomopathogenic fungus Clonostachys rosea on mortality rates and gene expression profiles in Diaphorina citri adults. Journal of Invertebrate Pathology, 179.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 Tatiana de Oliveira Portes; Ida Chapaval Pimentel; Maria Aparecida Cassilha Zawadneak
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
1) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
2) Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
3) Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.
