Exploring the impact of a chemical disinfectant and an antiviral drug for RNA virus management in the Mediterranean fruit fly mass-rearing

Abstract

The Mediterranean fruit fly is an agricultural pest of a wide variety of fruit crops. An effective method to counteract them in the field is through the application of the sterile insect technique, which requires the mass-production of sterile males. The presence of pathogens, and specifically viruses, threatens the well-being of mass-reared insects generating an interest on the development of strategies for viral elimination or containment. Thirteen RNA viruses have been described in the medfly although so far only one of them, Ceratitis capitata nora virus, has been associated with detrimental effects on medfly development. In this context, medfly larvae were supplied with a chemical compound (formaldehyde) and an antiviral compound (ribavirin) via oral feeding to (1) test the potential of these compounds for viral elimination and (2) analyze their effect on medfly development. Overall, formaldehyde treatment did not reduce the viral titer for any of the tested viruses, while ribavirin effectively reduced the levels of two widespread RNA viruses but not in a dose–response manner. However, the addition of both compounds correlated with detrimental effects on medfly fitness, arguing against their use in mass-rearing facilities.

Keywords

covert RNA virus / insect specific virus / mass-rearing / sterile insect technique / virus mitigation

References

[1] Abd-Alla, A.M.M. Adun, H. Parker, A.G. Vreysen, M.J.B. and Bergoin, M. (2012) The antiviral drug valacyclovir successfully suppresses salivary gland hypertrophy virus (SGHV) in laboratory colonies of Glossina pallidipes. PLoS ONE, 7, e38417.

[2] Agrawal, N. Dasaradhi, P.V.N. Mohmmed, A. Malhotra, P. Bhatnagar, R.K. and Mukherjee, S.K. (2003) RNA interference: biology, mechanism, and applications. Microbiology and Molecular Biology Reviews, 67, 657-685.

[3] Armién, A.G. Polon, R. Rejmanek, D. Moeller, R.B. and Crossley, B.M. (2023) Outbreak of densovirus with high mortality in a commercial mealworm (Tenebrio molitor) farm: a molecular, bright-field, and electron microscopic characterization. Veterinary Pathology, 60, 689-703.

[4] Dalmon, A. Gayral, P. Decante, D. Klopp, C. Bigot, D. Thomasson, M. et al. (2019) Viruses in the invasive hornet Vespa velutina. Viruses, 11, 1041.

[5] de Pedro, L. Harbi, A. Tormos, J. Sabater-Muñoz, B. and Beitia, F. (2021) A minor role of host fruit on the parasitic performance of Aganaspis daci (Hymenoptera: Figitidae) on medfly larvae. Insects, 12, 345.

[6] Dubey, S.K. and Das, P. (2021) Formaldehyde: risk assessment, environmental, and health hazard. In Hazardous Gases: Risk Assessment on the Environment and Human Health (eds. J. Singh, R.D. Kaushik & M. Chawla), pp. 169-182. Academic Press, New York, USA.

[7] Eilenberg, J. van Oers, M.M. Jensen, A.B. Lecocq, A. Maciel-Vergara, G. Santacoloma, L.P.A. et al. (2018) Towards a coordination of European activities to diagnose and manage insect diseases in production facilities. Journal of Insects As Food and Feed, 4, 157-166.

[8] Espino-Vázquez, A.N. Bermúdez-Barrientos, J.R. Cabrera-Rangel, J.F. Córdova-López, G. Cardoso-Martínez, F. Martínez-Vázquez, A. et al. (2020) Narnaviruses: novel players in fungal-bacterial symbioses. The ISME Journal, 14, 1743-1754.

[9] Haasnoot, J. Westerhout, E.M. and Berkhout, B. (2007) RNA interference against viruses: strike and counterstrike. Nature Biotechnology, 25, 1435-1443.

[10] Hajano, J.U.D. Raza, A. Zhang, L. Liu, W. and Wang, X. (2020) Ribavirin targets sugar transporter 6 to suppress acquisition and transmission of rice stripe tenuivirus by its vector Laodelphax striatellus. Pest Management Science, 76, 4086-4092.

[11] Hernández-Pelegrín, L. García-Martínez, R. Llácer, E. Nieves, L. Llopis-Giménez, Á. Catalá-Oltra, M. et al. (2024) Covert infection with an RNA virus affects medfly fitness and the interaction with its natural parasitoid Aganaspis daci. Journal of Pest Science, 97, 269-280.

[12] Hernández-Pelegrín, L. Llopis-Giménez, Á. Crava, C.M. Ortego, F. Hernández-Crespo, P. Ros, V.I.D. et al. (2022) Expanding the medfly virome: viral diversity, prevalence, and sRNA profiling in mass-reared and field-derived medflies. Viruses, 14, 623.

[13] Hernández-Pelegrín, L. Huditz, H. García-Castillo, P. de Ruijter, N.C.A. van Oers, M.M. Herrero, S. et al. (2024) Covert RNA viruses in medflies differ in their mode of transmission and tissue tropism. Journal of Virology, 98, e00108-e00124.

[14] Herrero, N. and Zabalgogeazcoa, I. (2011) Mycoviruses infecting the endophytic and entomopathogenic fungus Tolypocladium cylindrosporum. Virus Research, 160, 409-413.

[15] Herrero, S. Millán-Leiva, A. Coll, S. González-Martínez, R.M. Parenti, S. and González-Cabrera, J. (2019) Identification of new viral variants specific to the honey bee mite Varroa destructor. Experimental and Applied Acarology, 79, 157-168.

[16] Huynh, M.P. Shelby, K.S. and Coudron, T.A. (2021) Recent advances in insect rearing methodology to promote scientific research and mass production. Insects, 12, 961.

[17] Karl, A.R. Indira, K. Vinson, S.B. and Behmer, S.T. (2010) Evaluation of a microbial inhibitor in artificial diets of a generalist caterpillar, Heliothis virescens. Journal of Insect Science, 10, 197.

[18] Klassen, W. (2005) Area-wide integrated pest management and the sterile insect technique. In Sterile Insect Technique (eds. V.A. Dyck, J. Hendrichs & A.S. Robinson), pp. 39-68. Springer, Dordrecht, Netherlands.

[19] Kupke, P. Adenugba, A. Schemmerer, M. Bitterer, F. Schlitt, H.J. Geissler, E.K. et al. (2023) Immunomodulation of natural killer cell function by Ribavirin involves TYK-2 activation and subsequent increased IFN-γ Secretion in the context of in vitro Hepatitis E virus infection. Cells, 12, 453.

[20] Lin, Q. Lim, J.Y.C. Xue, K. Yew, P.Y.M. Owh, C. Chee, P.L. et al. (2020) Sanitizing agents for virus inactivation and disinfection. View, 1, e16.

[21] Llopis-Giménez, A. Maria González, R. Millán-Leiva, A. Catalá, M. Llacer, E. Urbaneja, A. et al. (2017) Novel RNA viruses producing simultaneous covert infections in Ceratitis capitata. Correlations between viral titers and host fitness, and implications for SIT programs. Journal of Invertebrate Pathology, 143, 50-60.

[22] Maciel-Vergara, G. and Ros, V.I.D. (2017) Viruses of insects reared for food and feed. Journal of Invertebrate Pathology, 147, 60-75.

[23] Martin, S.J. and Brettell, L.E. (2019) Deformed wing virus in honeybees and other insects. Annual Review of Virology, 6, 49-69.

[24] Möller, L. Schünadel, L. Nitsche, A. Schwebke, I. Hanisch, M. and Laue, M. (2015) Evaluation of virus inactivation by formaldehyde to enhance biosafety of diagnostic electron microscopy. Viruses, 7, 666-679.

[25] Morrow, J.L. Sharpe, S.R. Tilden, G. Wyatt, P. Oczkowicz, S. and Riegler, M. (2023) Transmission modes and efficiency of iflavirus and cripavirus in Queensland fruit fly, Bactrocera tryoni. Journal of Invertebrate Pathology, 197, 107874.

[26] Niu, J. Chen, R. and Wang, J.J. (2023) RNA interference in insects: the link between antiviral defense and pest control. Insect Science, 31, 2-12.

[27] Niu, Y. Zhang, T. Zhu, Y. Yuan, Y. Wang, S. Liu, J. et al. (2016) Isolation and characterization of a novel mycovirus from Penicillium digitatum. Virology, 494, 15-22.

[28] Parker, W.B. (2005) Metabolism and antiviral activity of ribavirin. Virus Research, 107, 165-171.

[29] Plá, I. García de Oteyza, J. Tur, C. Martínez, M.Á. Laurín, M.C. Alonso, E. et al. (2021) Sterile insect technique programme against Mediterranean fruit fly in the Valencian Community (Spain). Insects, 12, 415.

[30] Porras, M.F. Meza, J.S. Rajotte, E.G. Bourtzis, K. and Cáceres, C. (2020) Improving the phenotypic properties of the Ceratitis capitata (Diptera: Tephritidae) temperature-sensitive lethal genetic sexing strain in support of Sterile Insect Technique applications. Journal of Economic Entomology, 113, 2688-2694.

[31] Protano, C. Buomprisco, G. Cammalleri, V. Pocino, R.N. Marotta, D. Simonazzi, S. et al. (2021) The carcinogenic effects of formaldehyde occupational exposure: a systematic review. Cancers, 14, 165.

[32] Ricke, S.C. Richardson, K. and Dittoe, D.K. (2019) Formaldehydes in feed and their potential interaction with the poultry gastrointestinal tract microbial community—a review. Frontiers in Veterinary Science, 6, 188.

[33] Ryabov, E.V. (2017) Invertebrate RNA virus diversity from a taxonomic point of view. Journal of Invertebrate Pathology, 147, 37-50.

[34] Savio, C. Mugo, L. and Upfold, J. (2022) Bugs in bugs: The role of probiotics and prebiotics in maintenance of health in mass-reared insects. Insects, 13, 376.

[35] Sharpe, S.R. Morrow, J.L. Brettell, L.E. Shearman, D.C. Gilchrist, S. Cook, J.M. et al. (2021) Tephritid fruit flies have a large diversity of co-occurring RNA viruses. Journal of Invertebrate Pathology, 186, 107569.

[36] Shi, M. Lin, X.D. Tian, J.H. Chen, L.J. Chen, X. Li, C.X. et al. (2016) Redefining the invertebrate RNA virosphere. Nature, 540, 539-543.

[37] Tiring, G. and Satar, S. (2021) Annual population fluctuations of Mediterranean fruit fly in the Eastern Mediterranean Region of Turkey; problem of non-marketing fruit. Phytoparasitica, 49, 807-817.

[38] Toth, Jr, S.J,. (2009) Integrated pest management: concepts, tactics, strategies and case studies. In Integrated Pest Management: Concepts, Tactics, Strategies and Case Studies (eds. E.B. Radcliffe, W.D. Hutchinson & R.E. Cancelado), pp. 607-608. Cambridge University Press, Cambridge.

[39] Wu, H. Pang, R. Cheng, T. Xue, L. Zeng, H. Lei, T. et al. (2020) Abundant and diverse RNA viruses in insects revealed by RNA-Seq analysis: ecological and evolutionary implications. Msystems, 5, 4.

[40] Yuan, H. Xu, P. Xiao, Y. Yang, L. Yang, X. and Wu, K. (2020) Infection of cotton bollworm by Helicoverpa armigera iflavirus decreases larval fitness. Journal of Invertebrate Pathology, 173, 107384.

RIGHTS & PERMISSIONS

2024 The Author(s). Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.