Entomopathogenic fungi associated with whitefly control: A review

Authors

DOI:

https://doi.org/10.33448/rsd-v11i11.33536

Keywords:

Bemisia tabaci; Biological control; Beauveria bassiana; Cordyceps fumosorosea.

Abstract

Currently, the development and registration of a series of products based on Cordyceps fumosorosea and Beauveria bassiana have shown to be highly able to suppress and control whitefly under greenhouse and field conditions. However, some factors have weighed negatively on their use as slow action, low efficiency against adults and eggs, negative interaction with fungicides, and climatic limitations. Accordingly, studies have been developed to overcome those limitations, using several cultural practices to increase the efficiency of those organisms. Therefore, this review aims to list which entomopathogenic fungi have a control effect against Bemisia tabaci and what are the favourable conditions for this control. To that end, a literature review was carried out on scientific papers, analyzing studies with entomopathogenic fungi to control B. tabaci and those on the favourable environmental conditions for it, in addition to those that selected which instars are the most sensitive to the action of such control organisms. In conclusion, we may infer that B. tabaci can be managed by entomopathogenic fungi if the following measures are adopted: a) use against nymphal instars; b) use under favourable environmental conditions for the biological agents; c) use of application technology to increase the efficiency of the application of spores; and d) asynchronous application with fungicides. Furthermore, due to the innocuousness of these organisms, food and environmental security can also be increased.

References

Abd-Rabou, S., & Simmons, A. M. (2010). Survey of reproductive host plants of Bemisia tabaci (Hemiptera: Aleyrodidae) in Egypt, including new host records. Entomological news, 121(5), 456-465.

Azevedo, F. R. de, Guimarães, J. A., Braga Sobrinho, R., & Lima, M. A. A. (2005). Eficiência De Produtos Naturais Para O Controle De Bemisia Tabaci Biótipo B (Hemiptera: Aleyrodidae) Em Meloeiro. Arquivos do Instituto Biológico, 72(1), 73–79. https://doi.org/10.1590/1808-1657v72p0732005

Bethke, J. A., Paine, T. D., & Nuessly, G. S. (1991). Comparative biology, morphometrics, and development of two populations of Bemisia tabaci (Homoptera: Aleyrodidae) on cotton and poinsettia. Annals of the Entomological Society of America, 84(4), 407-411.

Biológico, S., & Paulo. (2006). (pp. 487–489). http://www.biologico.sp.gov.br/uploads/docs/bio/suplementos/v68_supl/p487-489.pdf

Boykin, L. M. (2014). Bemisia tabaci nomenclature: lessons learned. Pest management science, 70(10), 1454-1459.

Butler Jr, G. D., Henneberry, T. J., & Clayton, T. E. (1983). Bemisia tabaci (Homoptera: Aleyrodidae): development, Oviposition, and longevity in relation to temperature. Annals of the Entomological Society of America, 76(2), 310-313.

CABI, 2020 Center for Agriculture and Biosciences International, Invasive Species Compendium. Bemisia tabaci (tobacco whitefly). http://www.cabi.org/isc/datasheet/8927.

Candido, G. F. O. (2000). Virulence of the entomopathogenic fungus Paecilomyces amoenoroseus (Hennings) Samson toward the whitefly Bemisia argentifolii Bellows and Perring. Ph.D. Tese. University of California, USA.

Carruthers, R. I., Wraight, S. P., & Jones, W. A. (1993). An overview of biological control of the sweetpotato whitefly, Bemisia tabaci. In: Proceedings of the Beltwide Cotton Conference, 2, 680–685.

Castineiras, A. (1995). Natural enemies of Bemisia tabaci (Homoptera: Aleyrodidae) in Cuba. Florida Entomologist, 538-538.

Cock, M. J. W. (1993). Bemisia tabaci an UPDATE 1986-1992: on the cotton whitefly with an annotated bibliography (No. C059. 022). CAB International.

Coudriet, D. L., Prabhaker, N., Kishaba, A. N., & Meyerdirk, D. E. (1985). Variation in developmental rate on different hosts and overwintering of the sweetpotato whitefly, Bemisia tabaci (Homoptera: Aleyrodidae). Environmental Entomology, 14(4), 516-519.

Curnutte, L. B., Simmons, A. M., & Abd-Rabou, S. (2014). Climate change and Bemisia tabaci (Hemiptera: Aleyrodidae): impacts of temperature and carbon dioxide on life history. Annals of the Entomological Society of America, 107(5), 933-943.

Cuthbertson, A. G., Blackburn, L. F., Eyre, D. P., Cannon, R. J., Miller, J., & Northing, P. (2011). Bemisia tabaci: The current situation in the UK and the prospect of developing strategies for eradication using entomopathogens. Insect Science, 18(1), 1-10.

Cuthbertson, A. G., & Vänninen, I. (2015). The importance of maintaining protected zone status against Bemisia tabaci. Insects, 6(2), 432-441.

Dinsdale, A., Cook, L., Riginos, C., Buckley, Y. M., & De Barro, P. (2010). Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Annals of the Entomological Society of America, 103(2), 196-208.

Esashika, D. A, S., Michereff-Filho, M., Bastos, C. S., Inoue-Nagata, A. K., Dias, A. M., & Ribeiro, M. G. P. M. (2016). Suscetibilidade de adultos de Bemisia tabaci biótipo B a inseticidas. Horticultura Brasileira, 34(2), 189-195.

Eyal, J., Mabud, M. A., Fischbein, K. L., Walter, J. F., Osborne, L. S., & Landa, Z. (1994). Assessment of Beauveria bassiana Nov. EO-1 strain, which produces a red pigment for microbial control. Applied Biochemistry and Biotechnology, 44(1), 65-80.

Faria, M., & Wraight, S. P. (2001). Biological control of Bemisia tabaci with fungi. Crop protection, 20(9), 767-778.

Forza, C. (2002). Survey research in operations management: a process‐based perspective. International Journal of Operations & Production Management, 22(2), 152–194.

França, F. H., Boas, G. L. V., & Branco, M. C. (1996). Ocorrência de Bemisia argentifolii Bellows & Perring (Homoptera: Aleyrodidae) no Distrito Federal. Anais da Sociedade Entomologica do Brasil, 25, 369-72.

Garrido-Jurado, I., Resquín-Romero, G., Amarilla, S. P., Ríos-Moreno, A., Carrasco, L., & Quesada-Moraga, E. (2017). Transient endophytic colonization of melon plants by entomopathogenic fungi after foliar application for the control of Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae). Journal of Pest Science, 90(1), 319-330.

Ghahari, H., Abd-Rabou, S., Zahradnik, J., & Ostovan, H. (2013). Annotated catalogue of whiteflies (Hemiptera: Sternorrhyncha: Aleyrodidae) from Arasbaran, Northwestern Iran. Journal of Entomology and Nematology, 1(1), 007-018.

Ghosh, S., Kanakala, S., Lebedev, G., Kontsedalov, S., Silverman, D., Alon, T., & Mawassi, M. (2019). Transmission of a new polerovirus infecting pepper by the whitefly Bemisia tabaci. Journal of virology, 93(15), e00488-19.

Gill, R. J. (1990). The morphology of whiteflies. In: Whiteflies: Their Bionomics, Pest Status and Management. (pp. 13-46). Andover: Intercept.

Gondim, R. da S. (2021). Fungo Entomopatogênico Cordyceps fumosorosea NO Controle De Bemisia tabaci Em Feijoeiro Comum. Repositorio.ifgoiano.edu.br. https://repositorio.ifgoiano.edu.br/handle/prefix/2056

Goettel, M. S., Hajek, A. E., Siegel, J. P., & Evans, H. C. (2001). Safety of Fungal Biocontrol Agents. In: Fungi as biocontrol agents (pp. 347–376). Wallingford: CABI.

Guo, J. Y., Cong, L., Zhou, Z. S., & Wan, F. H. (2012). Multi-generation life tables of Bemisia tabaci (Gennadius) biotype B (Hemiptera: Aleyrodidae) under high-temperature stress. Environmental entomology, 41(6), 1672-1679.

Hai-lin, Y. A. N. G., Xiang-yong, L. I., Li-meng, Z. H. A. N. G., Yan-qiong, Y. I. N., Xue-qing, Z. H. A. O., & Ai-dong, C. H. E. N. (2014). Optimization for Bemisia tabaci egg development conditions using orthogonal design. Journal of Southern Agriculture, 45(11).

Inglis, G. D., Goettel, M. S., Butt, T. M., & Strasser, H. (2001). Use of hyphomycetous fungi for managing insect pests. In: Fungi as biocontrol agents (pp. 23-69). Wallingford: CABI.

James, R. R., Buckner, J. S., & Freeman, T. P. (2003). Cuticular lipids and silverleaf whitefly stage affect conidial germination of Beauveria bassiana and Paecilomyces fumosoroseus. Journal of Invertebrate Pathology, 84(2), 67-74.

Kakimoto, K., Inoue, H., Yamaguchi, T., Ueda, S., Honda, K. I., & Yano, E. (2007). Host plant effect on development and reproduction of Bemisia argentifolii Bellows and Perring (B. tabaci [Gennadius] B-biotype) (Homoptera: Aleyrodidae). Applied entomology and zoology, 42(1), 63-70.

Lacey, L. A., Kirk, A. A., & Hennessey, R. D. (1993). Foreign exploration for natural enemies of Bemisia tabaci and implementation in integrated control programs in the United States. In: Proceedings, Third International Conference on Pests in Agriculture. 351–360.

Lacey, L. A., Fransen, J. J., & Carruthers, R. (1996). Global distribution of naturally occurring fungi of Bemisia, their biologies and use as biological control agents. In: Bemisia 1995- Taxonomy, Biology, Damage, Control and Management (pp. 401–433). Andover: Intercept.

Lacey, L. A., Kirk, A. A., Millar, L., Mercadier, G., & Vidal, C. (1999). Ovicidal and larvicidal activity of conidia and blastospores of Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes) against Bemisia argentifolii (Homoptera: Aleyrodidae) with a description of a bioassay system allowing prolonged survival of control insects. Biocontrol Science and Technology, 9(1), 9-18.

Fransen, J. J., 1990. Natural enemies of whiteflies: fungi. In: Whiteflies, their Bionomics, Pest Status and Management. (pp. 187–210). Andover: Intercept.

Lima, C. H., Sarmento, R. A., Pereira, P. S., Galdino, T. V., Santos, F. A., Silva, J., & Picanço, M. C. (2017). Feasible sampling plan for Bemisia tabaci control decision‐making in watermelon fields. Pest management science, 73(11), 2345-2352.

Lima, C. H., Sarmento, R. A., Galdino, T. V., Pereira, P. S., Silva, J., Souza, D. J., & Picanço, M. C. (2018). Spatiotemporal dynamics of whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) in commercial watermelon crops. Journal of economic entomology, 111(4), 1895-1903.

López, V., Vos, J., Polar, P., & Krauss, U. Discovery learning about sustainable management of whitefly pests and whitefly-borne viruses. International Centre for Tropical Agriculture (CIAT), 1(1), 12-37.

Lorenzo, M. E., Grille, G., Basso, C., & Bonato, O. (2016). Host preferences and biotic potential of Trialeurodes vaporariorum and Bemisia tabaci (Hemiptera: Aleyrodidae) in tomato and pepper. Arthropod-Plant Interactions, 10(4), 293-301.

Lourenção, A. L., & Nagai, H. (1994). Surtos populacionais de Bemisia tabaci no Estado de São Paulo. Bragantia, 53(1), 53-59.

Maranhão, E. A. D. A., Maranhão, E. H. D. A., & de Oliveira, N. Eficácia de fungos entomopatógenos contra Bemisia tabaci biótipo B em cultivo de tomate sob condições de telado. Horticultura Brasileira, 29(2), S544-S551.

Macías, A. F., Díaz, M. P., Ramos-López, M. A., Navarro, S. R., Espinosa, G. R., & Ruiz, D. J. (2013). Estudio del hongo entomopatógeno Isaria fumosorosea como control microbiológico de la mosquita blanca Bemicia tabaci. Interciencia, 38(7), 523-527.

McKenzie, C. L., Kumar, V., Palmer, C. L., Oetting, R. D., & Osborne, L. S. (2014). Chemical class rotations for control of Bemisia tabaci (Hemiptera: Aleyrodidae) on poinsettia and their effect on cryptic species population composition. Pest management science, 70(10), 1573-1587.

Meade, D. L., & Byrne, D. N. (1991). The use of Verticillium lecanii against subimaginal instars of Bemisia tabaci. Journal of Invertebrate Pathology, 57(2), 296-298.

Nava-Camberos, U., Riley, D. G., & Harris, M. K. (2001). Temperature and host plant effects on development, survival, and fecundity of Bemisia argentifolii (Homoptera: Aleyrodidae). Environmental Entomology, 30(1), 55-63.

Navas-Castillo, J., Fiallo-Olivé, E., & Sánchez-Campos, S. (2011). Emerging virus diseases transmitted by whiteflies. Annual review of phytopathology, 49, 219-248.

Naranjo, S. E., Castle, S. J., De Barro, P. J., & Liu, S. S. (2010). Population dynamics, demography, dispersal and spread of Bemisia tabaci. In Bemisia: Bionomics and management of a global pest (pp. 185-226). Dordrecht: Springer.

Negasi, A., Parker, B. L., & Brownbridge, M. (1998). Screening and bioassay of entomopathogenic fungi for the control of silverleaf whitefly, Bemisia argentifolli. International Journal of Tropical Insect Science, 18(1), 37-44.

Perring, T. M., Cooper, A., & Kazmer, D. J. (1992). Identification of the poinsettia strain of Bemisia tabaci (Homoptera: Aleyrodidae) on broccoli by electrophoresis. Journal of Economic Entomology, 85(4), 1278-1284.

Perring, T. M., Cooper, A. D., Rodriguez, R. J., Farrar, C. A., & Bellows, T. S. (1993). Identification of a whitefly species by genomic and behavioral studies. Science, 259(5091), 74-77.

Perring, T. M., Stansly, P. A., Liu, T. X., Smith, H. A., & Andreason, S. A. (2018). Whiteflies: biology, ecology, and management. In: Sustainable Management of Arthropod Pests of Tomato (pp. 73-110). Cambridge: Academic Press.

Potrich, M., Neves, P. M. O. J., Alves, L. F. A., Pizzatto, M., Silva, E. R. L., Luckmann, D., & Roman, J. C. (2011). Virulence of entomopathogenic fungi against nymphs of Bemisia tabaci (Genn.) (Hemiptera: Aleyrodidae). Semina: Ciências Agrárias, 32(4Sup1), 1783-1792.

Ramos, E. Q., Alves, S. B., Tanzini, M. R., & Lopez, R. B. (2000). Susceptibilidad de Bemisia tabaci a Beauveria bassianaa en condiciones de laboratorio. CATIE, Turrialba (Costa Rica).

Sampaio, R. F., & Mancini, M. C. (2007). Estudos de revisão sistemática: um guia para síntese criteriosa da evidência científica. Brazilian Journal of Physical Therapy, 11(1), 83-89.

Silva, A. G. D., Boiça Junior, A. L., Farias, P. R. S., & Barbosa, J. C. (2011a). Infestação da mosca-negra-dos-citros (Aleurocanthus woglumi Ashby) em pomares de citros, em sistemas de plantio convencional e agroflorestal. Revista Brasileira de Fruticultura, 53-60.

Silva, A. G., Junior, A. L. B., Farias, P. R. S., Rodrigues, N. E. L., Monteiro, B. S., & Santos, N. A. (2011b). Influência de fatores abióticos na infestação de mosca-negra-dos-citros (Aleurocanthus woglumi Ashby) em plantio de citros em sistema agroflorestal no estado do Pará. EntomoBrasilis, 4(1), 01-06.

Silva, A. G., Junior, A. L. B., Farias, P. R. S., de Souza, B. H. S., Rodrigues, N. E. L., & de Jesus, F. G. (2014). Dinâmica populacional de mosca-branca Bemisia tabaci (Genn.) Biótipo B (Hemiptera: Aleyrodidae) em feijoeiro. EntomoBrasilis, 7(1), 05-11.

Silva, A. G., Junior, A. L. B., de Souza, B. H. S., Costa, E. N., da Silva Hoelhert, J., Almeida, A. M., & dos Santos, L. B. (2017). Mosca-Branca, Bemisia tabaci (Genn.) (Hemiptera: Aleyrodidae) em feijoeiro: Características gerais, bioecologia e métodos de controle. EntomoBrasilis, 10(1), 01-08.

Souza, G., L. (2022). Ação de bioinseticidas formulados a partir de fungos entomopatogênicos sobre diferentes fases de desenvolvimento de Brevicoryne brassicae (Linnaeus) e biologia comparada com Lipaphis pseudobrassicae (Davis) (Hemiptera: Aphididae). https://repositorio.ufsc.br/handle/123456789/235162

Stansly, P. A., & Natwick, E. T. (2009). Integrated systems for managing Bemisia tabaci in protected and open field agriculture. In Bemisia: Bionomics and management of a global pest (pp. 467-497). Dordrecht: Springer.

Stansly, P. A., & Naranjo, S. E. (2010). Bemisia: bionomics and management of a global pest. Berlin: Springer Science & Business Media.

Vestergaard, S., Cherry, A., Keller, S., & Goettel, M. (2003). Safety of hyphomycete fungi as microbial control agents. In Environmental impacts of microbial insecticides (pp. 35-62). Dordrecht: Springer.

Vicentini, S., Faria, M., & de Oliveira, M. R. (2001). Screening of Beauveria bassiana (Deuteromycotina: Hyphomycetes) isolates against nymphs of Bemisia tabaci (Genn.) biotype B (Hemiptera: Aleyrodidae) with description of a new bioassay method. Neotropical Entomology, 30(1), 97-103.

Vidal, C., Fargues, J., Rougier, M., & Smits, N. (2003). Effect of air humidity on the infection potential of hyphomycetous fungi as mycoinsecticides for Trialeurodes vaporariorum. Biocontrol Science and Technology, 13(2), 183-198.

Villas Bôas, G. L., França, F. H., De Ávila, A. C., & Bezerra, I. C. (1997). Manejo integrado da mosca-branca Bemisia argentifolii. EMBRAPA-CNPH. Circular Técnica da Embrapa Hortaliças.

Walker, G. P., Perring, T. M., & Freeman, T. P. (2010). Life history, functional anatomy, feeding and mating behavior. In Bemisia: Bionomics and management of a global pest (pp. 109-160). Dordrecht: Springer.

Wang, L., Huang, J., You, M., Guan, X., & Liu, B. (2007). Toxicity and feeding deterrence of crude toxin extracts of Lecanicillium (Verticillium) lecanii (Hyphomycetes) against sweet potato whitefly, Bemisia tabaci (Homoptera: Aleyrodidae). Pest Management Science: formerly Pesticide Science, 63(4), 381-387.

Wraight, S. P., Carruthers, R., Bradley, C. A., Jaronski, S. T., Lacey, L. A., Wood, P., & Galaini-Wraight, S. (1998). Pathogenicity of the Entomopathogenic Fungi Paecilomyces spp. And Beauveria bassiana gainst the Silverleaf Whitefly, Bemisia argentifolii. Journal of Invertebrate Pathology, 71(3), 217-226.

Wraight, S. P., & Carruthers, R. I. (1999). Production, delivery, and use of mycoinsecticides for control of insect pests on field crops. In: Biopesticides: use and Delivery (pp. 233-269). Totowa: Humana Press.

Wraight, S. P., Carruthers, R. I., Jaronski, S. T., Bradley, C. A., Garza, C. J., & Galaini-Wraight, S. (2000). Evaluation of the entomopathogenic fungi Beauveria bassiana and Paecilomyces fumosoroseus for microbial control of the silverleaf whitefly, Bemisia argentifolii. Biological control, 17(3), 203-217.

Yang, T. C., & Chi, H. (2006). Life tables and development of Bemisia argentifolii (Homoptera: Aleyrodidae) at different temperatures. Journal of Economic Entomology, 99(3), 691-698.

Zaidi, S. S. E. A., Briddon, R. W., & Mansoor, S. (2017). Engineering dual begomovirus-Bemisia tabaci resistance in plants. Trends in plant science, 22(1), 6-8.

Zimmermann, G. (2008). The entomopathogenic fungi Isaria farinosa (formerly Paecilomyces farinosus) and the Isaria fumosorosea species complex (formerly Paecilomyces fumosoroseus): biology, ecology and use in biological control. Biocontrol science and technology, 18(9), 865-901.

Published

21/08/2022

How to Cite

SOUZA, F. M. de; SILVA, R. A. da .; MAGALHÃES, L. da S.; LOUREIRO, E. de S. . Entomopathogenic fungi associated with whitefly control: A review. Research, Society and Development, [S. l.], v. 11, n. 11, p. e252111133536, 2022. DOI: 10.33448/rsd-v11i11.33536. Disponível em: https://www.rsdjournal.org/index.php/rsd/article/view/33536. Acesso em: 25 apr. 2024.

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Agrarian and Biological Sciences