Intraspecific virulence of entomopathogenic nematodes against the pests Frankliniella occidentalis (Thysanoptera: Thripidae) and Tuta absoluta (Lepidoptera: Gelechiidae)

Campos-Herrera, Raquel; Vicente-Díez, Ignacio; Galeano, Magda; Chelkha, Maryam; del Mar González-Trujillo, María; Puelles, Miguel; Labarga, David; Pou, Alicia; Calvo, Javier; Belda, José Eduardo

doi:10.21307/jofnem-2021-102

Abstract

Entomopathogenic nematodes (EPN) are excellent biocontrol agents against various insect pests. Novel biotechnological approaches can enhance their utility against insects above-ground, opening a new venue for selecting superior EPN against certain insects. We hypothesize that different populations of the same species but from different origins (habitat, ecoregion) will differ in their virulence. This study aimed to evaluate the virulence of various EPN populations against two pests of worldwide incidence and damage to high value crops: Frankliniella occidentalis (Thysanoptera: Thripidae) and Tuta absoluta (Lepidoptera: Gelechiidae). We tested 10 EPN populations belonging to three EPN species: Heterorhabditis bacteriophora (Koppert, MG-618b, AM-203, RM-102), Steinernema feltiae (Koppert, RS-5, AM-25, RM-107), and Steinernema carpocapsae (Koppert, MG-596a). Each EPN population was tested at two concentrations. Frankliniella occidentalis was tested at 160 and 80 IJs/cm² and T. absoluta at 21 and 4 IJs/cm². Control treatments followed the same experimental procedure but only adding distilled water. Overall, whenever different, higher IJs concentration resulted in lower adult emergence, higher larval mortality, and shorter time to kill the insects. Considering the low concentration, S. feltiae provided the best results for both insects and instars investigated, while H. bacteriophora and S. carpocapsae required a high concentration to reach similar or slightly better results. Differences among populations of each of the species were detected, but only the native populations of H. bacteriophora populations showed consistently higher control values against both insects/instar compared with the commercial one. Differences among S. feltiae and S. carpocapsae populations depended on the IJs concentration, insect, and instar. We consider S. feltiae a very promising species for their application against F. occidentalis and T. absoluta, with the Koppert population as the most consistent among the populations tested. Specific EPN-populations of S. carpocapsae and H. bacteriophora were good candidates against certain instar/insects at high concentrations. This study emphasized the importance of intraspecific variability for EPN virulence.

References

Adams, B. J., Fodor, A., Koppenhöfer, H. S., Stackenbrandt, E., Stock, S. P. and Klein, G. 2006. Biodiversity and systematic of nematode-bacterium entomopathogens. Biological Control 38:4–21.
Search in Google Scholar Back to article
Batalla-Carrera, L., Morton, A. and Garcia-del-Pino, F. 2010. Efficacy of entomopathogenic nematodes against the tomato leafminer Tuta absoluta in laboratory and greenhouse conditions. BioControl 55:523–530.
Search in Google Scholar Back to article
Belay, D., Ebssa, L. and Borgemeister, C. 2005. Time and frequency of applications of entomopathogenic nematodes and their persistence for control of western flower thrips Frankliniella occidentalis. Nematology 7:611–622.
Search in Google Scholar Back to article
Ben Husin, T. O. and Port, G. R. 2021. Efficacy of entomopathogenic nematodes against Tuta absoluta. Biological Control 160:104699.
Search in Google Scholar Back to article
Biondi, A., Guedes, R. N. C., Wan, F. -H. and Desneux, N. 2018. Ecology, worldwide spread, and management of the invasive South American tomato pinworm, Tuta absoluta: past, present, and future. Annual Revue Entomology 63:239–258.
Search in Google Scholar Back to article
Bode, H. B. 2009. Entomopathogenic bacteria as a source of secondary metabolites. Current Opinion in Chemical Biology 13:224–230.
Search in Google Scholar Back to article
Brødsgaard, H. F. 2004. Biological control of thrips on ornamental crops. Journal of Economic Entomology 98:253–264.
Search in Google Scholar Back to article
Bruno, P., Machado, A. R., Glauser, G., Köhler, A., Campos-Herrera, R., Bernal, J., Toepfer, S., Erb, M., Robert, C. A. M., Arce, C. C. M. and Turlings, T. C. J. 2020. Entomopathogenic nematodes from Mexico that can overcome the resistance mechanisms of the western corn rootworm. Scientific Reports 10:8257.
Search in Google Scholar Back to article
Buitenhuis, R. and Shipp, J. L. 2005. Efficacy of entomopathogenic nematode Steinernema feltiae (Rhabditida: Steinernematidae) as influenced by Frankliniella occidentalis (Thysanoptera: Thripidae) developmental stage and host plant stage. Journal of Economic Entomology 98:1480–1485.
Search in Google Scholar Back to article
Campbell, J. F., Lewis, E. E., Stock, S. P., Nadler, S. and Kaya, H. K. 2003. Evolution of host search strategies in entomopathogenic nematodes. Journal of Nematology 35:142–145.
Search in Google Scholar Back to article
Campos-Herrera, R., Escuer, M., Labrador, S., Robertson, L., Barrios, L. and Gutiérrez, C. 2007. Distribution of the entomopathogenic nematodes from La Rioja (Northern Spain). Journal of Invertebrate Pathology 95:125–139.
Search in Google Scholar Back to article
Campos-Herrera, R., Gómez-Ros, J. M., Escuer, M., Cuadra, L., Barrios, L. and Gutiérrez, C. 2008. Diversity, occurrence, and life characteristics of natural entomopathogenic nematode populations from La Rioja (Northern Spain) under different agricultural management and their relationships with soil factors. Soil Biology and Biochemistry 40:1470–1484.
Search in Google Scholar Back to article
Campos-Herrera, R. and Gutierrez, C. 2009. Screening Spanish isolates of steinernematid nematodes for use as biological control agents through laboratory and greenhouse microcosm studies. Journal of Invertebrate Pathology 100:100–105.
Search in Google Scholar Back to article
Campos-Herrera, R., Tailliez, P., Pagès, S., Ginibre, N., Gutiérrez, C. and Boemare, N. E. 2009. Characterization of Xenorhabdus isolates from La Rioja (Northern Spain) and virulence with and without their symbiotic entomopathogenic nematodes (Nematoda: Steinernematidae). Journal of Invertebrate Pathology 102:173–181.
Search in Google Scholar Back to article
Campos-Herrera, R. and Gutiérrez, C. 2014. Steinernema feltiae intraspecific variability: infection process and sex–ratio. Journal of Nematology 46:35–43.
Search in Google Scholar Back to article
Campos-Herrera, R.“Nematode pathogenesis of insects and other pests”, Ecology and applied technologies for sustainable plant and crop protection Switzerland: Springer International Publishing, p. 531.
Search in Google Scholar Back to article
Campos-Herrera, R., Vicente-Díez, I., Blanco-Pérez, R., Chelkha, M., González-Trujillo, M. M., Puelles, M., Cepulite, R. and Pou, A. 2021. Positioning entomopathogenic nematodes for the future viticulture: exploring their use against biotic threats and as bioindicators of soil health. Turkish Journal of Zoology 45:335–346.
Search in Google Scholar Back to article
Chiriboga, X., Campos-Herrera, R., Jaffuel, G., Röder, G. and Turlings, T. C. J. 2017. Diffusion of the maize root signal (E)-β -caryophyllene in soils of different textures and the effects on the migration of the entomopathogenic nematode Heterorhabditis megidis. Rhizosphere 3:53–59.
Search in Google Scholar Back to article
Chyzik, R., Glazer, I. and Klein, M. 1996. Virulence and efficacy of different entomopathogenic nematode species against western flower thrips (Frankliniella occidentalis). Phytoparasitica 24:103–110.
Search in Google Scholar Back to article
Damalas, C. A. and Koutroubas, S. D. 2018. Current status and recent developments in biopesticide use. Agriculture 8:3.
Search in Google Scholar Back to article
Dillman, A. R., Chaston, J. M., Adams, B. J., Ciche, T. A., Goodrich-Blair, H., Stock, S. P. and Sternberg, P. W. 2012. An entomopathogenic nematode by any other name. PLoS Pathogens 8:e1002527.
Search in Google Scholar Back to article
Dlamini, T. M., Allshopp, E. and Malan, A. P. 2019a. Entomopathogenic nematodes to control of western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae), under laboratory conditions. African Entomology 27:322–335.
Search in Google Scholar Back to article
Dlamini, T. M., Allshopp, E. and Malan, A. P. 2019b. Management of Frankliniella occidentalis (western flower thrips), and the potential use of entomopathogenic nematodes: a South African perspective. African Entomology 27:265–278.
Search in Google Scholar Back to article
Dlamini, T. M., Allshopp, E. and Malan, A. P. 2020. Application of Steinernema yirgalemense to control Frankliniella occidentalis (Thysanoptera: Thripidae) on blueberries. Crop Protection 128:105016.
Search in Google Scholar Back to article
Ebssa, L., Borgemeister, C., Berndt, O. and Poehling, H. M. 2001. Efficacy of entomopathogenic nematodes against soil-dwelling life stages of western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae). Journal of Invertebrate Pathology 78:119–127.
Search in Google Scholar Back to article
Ebssa, L., Borgemeister, C., Berndt, O. and Poehling, H. M. 2004. Effectiveness of different species/strains of entomopathogenic nematodes for control of western flower thrips (Frankliniella occidentalis) at various concentrations, host densities, and temperatures. Biological Control 29:145–154.
Search in Google Scholar Back to article
Ebssa, L., Borgemeister, C. and Poehling, H. M. 2006. Simultaneous application of entomopathogenic nematodes and predatory mites to control western flower thrips Frankliniella occidentalis. Biological Control 39:66–74.
Search in Google Scholar Back to article
Elhady, A., Adss, S., Hallmann, J. and Heuer, H. 2018. Rhizosphere microbiomes modulated by precrops assisted plants in defense against plant-parasitic nematodes. Frontiers in Microbiology 9:1133.
Search in Google Scholar Back to article
Gao, Y. L., Lei, Z. R. and Reitz, S. R. 2012. Western flower thrips resistance to insecticides: detection, mechanisms and management strategies. Pest Management Science 68:1111–1124.
Search in Google Scholar Back to article
Gerritsen, L. J. M., Georgieva, J. and Wiegers, G. L. 2005. Oral toxicity of Photorhabdus toxins against thrips species. Journal of Invertebrate Pathology 88:207–211.
Search in Google Scholar Back to article
Gouli, S., Gouli, V., Skinner, M., Parker, B., Marcelino, J. and Shternshis, M. 2008. Mortality of western flower thrips, Frankliniella occidentalis, under influence of single and mixed fungal inoculations. Journal of Agricultural Technology 4:37–47.
Search in Google Scholar Back to article
Gözel, Ç. and Kasap, I. 2015. Efficacy of entomopathogenic nematodes against the Tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in tomato field. Turkish. Journal of Entomology 39:229–237.
Search in Google Scholar Back to article
Grewal, P. S., Bornstein-Forst, S., Burnell, A. M., Glazer, I. and Jagdale, G. B. 2006. Physiological, genetic, and molecular mechanisms of chemoreception, thermobiosis, and anhydrobiosis in entomopathogenic nematodes. Biological Control 38:54–65.
Search in Google Scholar Back to article
Griffin, C. T. 2015. Behaviour and population dynamics of entomopathogenic nematodes following application. Campos-Herrera, R.Nematode pathogenesis of insects and other pests: ecology and applied technologies for sustainable plant and crop protection. Springer International Publishing, AG Switzerland, pp. 57–95.
Search in Google Scholar Back to article
Kaya, H. K., Aguillera, M. M., Alumai, A., Choo, H. Y., de la Torre, M., Fodor, A., Ganguly, S., Hazir, S., Lakatos, T., Pye, A., Wilson, M., Yamanaka, S., Yang, H. and Ehlers, R. -U. 2006. Status of entomopathogenic nematodes and their symbiotic bacteria from selected countries or region of the world. Biological Control 38:134–155.
Search in Google Scholar Back to article
Lacey, L. A., Grzywacz, D., Shapiro-Ilan, D. I., Frutos, R., Brownbridge, M. and Goettel, M. S. 2015. Insect pathogens as biological control agents: Back to the future. Journal of Invertebrate Pathology 132:1–41.
Search in Google Scholar Back to article
Lee, S. J., Kim, S., Kim, J. C., Lee, M. R., Hossain, M. S., Shin, T. S., Kim, T. H. and Kim, J. S. 2017. Entomopathogenic Beauveria bassiana granules to control soil-dwelling stage of western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae). Biocontrol 62:639–648.
Search in Google Scholar Back to article
Levy, N., Faigenboim, A., Salame, L., Molina, C., Ehlers, R. U., Glazer, I. and Ment, D. 2020. Characterization of the phenotypic and genotypic tolerance to abiotic stresses of natural populations of Heterorhabditis bacteriophora. Scientific Reports 10:10500.
Search in Google Scholar Back to article
Mansour, R., Brévault, T., Chailleux, A., Cherif, A., Grissa-Lebdi, K., Haddi, K., Mohamed, S. A., Nofemela, R. S., Oke, A., Sylla, S., Tonnang, H. E. Z., Zappalà, L., Kenis, M., Desneux, N. and Biondi, A. 2018. Occurrence, biology, natural enemies and management of Tuta absoluta in Africa. Entomologia Generalis 38:83–112.
Search in Google Scholar Back to article
Mansour, R. and Biondi, A. 2020. Releasing natural enemies and applying microbial and botanical pesticides for managing Tuta absoluta in the MENA region. Phytoparasitica 49:179–194.
Search in Google Scholar Back to article
Messelink, G. J. and Janssen, A. 2014. Increased control of thrips and aphids in greenhouses with two species of generalist predatory bugs involved in intraguild predation. Biological Control 79:1–7.
Search in Google Scholar Back to article
Moritz, G. S., Kumm, S. and Mound, L. 2004. Tospovirus transmission depends on thrips ontogeny. Virus Research 100:143–149.
Search in Google Scholar Back to article
Mutegi, D. M., Kilalo, D., Kimenju, J. W. and Waturu, C. 2017. Pathogenicity of selected native entomopathogenic nematodes against tomato leaf miner (Tuta absoluta) in kenya. World Journal of Agricultural Research 5:233–239.
Search in Google Scholar Back to article
Premachandra, W. T., Borgemeister, C., Berndt, O., Ehlers, R. U. and Poehling, H. M. 2003. Combined releases of entomopathogenic nematodes and the predatory mite Hypoaspis aculeifer to control soil-dwelling stages of western flower thrips Frankliniella occidentalis. Biocontrol 48:529–541.
Search in Google Scholar Back to article
Shamseldean, M. S. M., Abd-Elbary, N. A., Shalaby, H. and Ibraheem, H. I. H. 2014. Entomopathogenic nematodes as biocontrol agents of the tomato leaf miner Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) on tomato plants. Egyptian. Journal of Biological Pest Control 24:503–513.
Search in Google Scholar Back to article
Shapiro-Ilan, D. I. and Dolinski, C. 2015. “Entomopathogenic nematode application technology”. Campos-Herrera, R.Nematode Pathogenesis of Insects and Other Pests, Sustainability in Plant and Crop Protection, Vol. 1, Springer International Publishing, Switzerland, pp. 231–254.
Search in Google Scholar Back to article
Shipp, J. L., Ramakers, P. M. 2004. Biological control of thrips on vegetable crops. Heinz, K. M., Van Driesche, R. G. and Parella, M. P.Biocontrol in Protected Culture. Ball, Batavia, IL, pp. 265–276.
Search in Google Scholar Back to article
Siguna, A. D.2007. Cultural and Botanical Methods for the Management of Thrips on French Beans Phaseolus vulgaris. Thesis MSc Agricultural Entomology. School of Pure and Applied Sciences, Kenyatta University, Nairobi. Available at: http://hdl.handle.net/123456789/137.
Search in Google Scholar Back to article
Stock, S. P. 2015. “Diversity, biology and evolutionary relationships”. Campos- Herrera, R.Nematode Pathogeneses of Insects and Other Pests Springer International Publishing, Switzerland, pp. 3–27.
Search in Google Scholar Back to article
Terzidis, A. N., Wilcockson, S. and Leifert, C. 2014. The tomato leaf miner (Tuta absoluta): conventional pest problem, organic management solutions. Organic Agriculture 4:43–61.
Search in Google Scholar Back to article
Trdan, S., Znidarcic, D. and Vidrih, M. 2007. Control of Frankliniella occidentalis on glasshouse-grown cucumbers: an efficacy comparison of foliar application of Steinernema feltiae and spraying with abamectin. Russian Journal of Nematology 15:25–34.
Search in Google Scholar Back to article
Urbaneja, A., González-Cabrera, J., Arnó, J. and Gabarra, R. 2012. Prospects for the biological control of Tuta absoluta in tomatoes of the Mediterranean basin. Pest Management Science 68:1215–1222.
Search in Google Scholar Back to article
Urbaneja, A., Desneux, N., Gabarra, R., Arnó, J., González-Cabrera, J., Mafra-Neto, A., Stoltman, L., De Sene Pinto, A. and Parra, J. R. P. 2013. Biology, ecology and management of the south american tomato pinworm, Tuta absoluta. Peña, J. E. Potential Invasive Pests of Agricultural Crops. CABI Publishing, Wallingford, pp. 98–125.
Search in Google Scholar Back to article
van Damme, V., Beck, B. K., Berckmoes, E., Moerjens, R., Wittemans, L., de Vis, R., Nuyttens, D., Casteels, H. F., Maes, M., Tirry, L. and de Clercq, P. 2013. Efficacy of entomopathogenic nematodes against larvae of Tuta absoluta in the laboratory. Pest Management Science 72:1702–1709.
Search in Google Scholar Back to article
Wardlow, L. R., Piggott, S. and Goldsworthy, R. 2001. Foliar application of Steinernema feltiae for the control of flower thrips. Mededelingen – Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen 66:285–291.
Search in Google Scholar Back to article
Woodring, J. L. and Kaya, H. K. 1988. Steinernematid and Heterorhabditid nematodes: a handbook of biology and techniques Southern Cooperative Series. Arkansas Agricultural Experiment Station, Arkansas. Series, Bulletin 331:30.
Search in Google Scholar Back to article
Zhao, G. Y., Liu, W., Brown, J. M. and Knowles, C. O. 1995. Insecticide resistance in-field and laboratory strains of western flower thrips (Thysanoptera, Thripidae). Journal of Economic Entomology 88:1164–1170.
Search in Google Scholar Back to article

Intraspecific virulence of entomopathogenic nematodes against the pests Frankliniella occidentalis (Thysanoptera: Thripidae) and Tuta absoluta (Lepidoptera: Gelechiidae)

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