The Efficiency of Aboriginal Entomopathogenic Nematodes from Semi-Arid Zone Against Tenebrionidae Larvae with Comparison to Commercial Bio-Insecticides

Dauren Kaliaskar, Aigerim Shibaeva, Nariman Zhappar, Valentin Shaikhutdinov, Laura Asherbekova, Sayakhat Bekbulatov, Almagul Kalyaskarova


Chemical insecticides are intensively used in agriculture which cause negative effects on environmental sustainability by increasing pest tolerance and continuous action on local fauna. In contrast to chemical insecticides, biological insecticides target specific pests, minimizing their impact on the surrounding environment. However, most of the natural insecticides available in the market are expensive for farmers in the Central Asian region. This study is the first evidence of the effectiveness of local entomopathogenic nematodes (EPN) from the arid zone of northern Kazakhstan that can be used as an alternative to export EPN products. The laboratory experiment is conducted with two local and two commercial Steinernema feltiae and Steinernema carpocapsae, which are applied to larvae of Tenebrionidae. The experiment design is randomized with four doses of EPN (100, 200, 300, and 400 IJ/cm2) and a control (without EPN). According to the experiment results, one out of two local EPNs (AF29 at dose 100 IJ/cm2) caused a high mortality rate (67%) among larvae. This finding confirms that local EPNs can compete with commercial EPNs and potentially be used as insecticidal agents.


Biological control insect pest; Entomopathogenic nematodes; Non-chemical pest control

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Acharya, R., Hwang, H.-S., Mostafiz, Md. M., Yu, Y.-S., & Lee, K.-Y. (2020). Susceptibility of various developmental stages of the fall armyworm, Spodoptera frugiperda, to entomopathogenic nematodes. Insects, 11(12), 868. DOI

Aipova, R., Abdykadyrova, A. B., & Kurmanbayev, A. A. (2019). Biological products in organic agriculture. Plant Biotechnology and Breeding, 2(4), 36–41. DOI

Akhurst, R., & Smith, K. (2002). Regulation and safety. In R. Gaugler (Ed.), Entomopathogenic nematology (pp. 311–332). Wallingford: CABI Publishing. Retrieved from website

Alves, V. S., De O. Neves, P. M. J., Alves, L. F. A., Moino Jr, A., & Holz, N. (2012). Entomopathogenic nematodes (Rhabditida: Heterorhabditidae and Steinernematidae) screening for lesser mealworm Alphitobius diaperinus (Coleoptera: Tenebrionidae) control. Revista Colombiana de Entomologia, 38(1), 76–80. Retrieved from website

Askary, T. H. (2010). Nematodes as biocontrol agents. In E. Lichtfouse (Ed.), Sociology, organic farming, climate change and soil science (pp. 347–378). Sustainable Agriculture Reviews, vol 3. Dordrecht: Springer. DOI

Askary, T. H., Nermuthacek˜, J., Ahmad, M. J., & Ganai, M. A. (2017). Future thrusts in expanding the use of entomopathogenic and slug parasitic nematodes in agriculture. In Biocontrol Agents: Entomopathogenic and Slug Parasitic Nematodes (pp. 620–628). DOI

Baliadi, Y., Sastrahidayat, I. R., Djauhari, S., & Rahardjo, B. T. (2011). Pathogenicity, development and reproduction of the entomopathogenic nematode Steinernema sp., in mealworm Tenebrio molitor. AGRIVITA Journal of Agricultural Science, 33(3), 233–244. Retrieved from website

Bechinski, E. J., Sandvol, L. E., Carpenter, G. P., & Homan, H. W. (1994). Integrated pest management guide to wireworms in potatoes (Bulletin no. 760). University of Idaho, College of Agriculture, Cooperative Extension System. Retrieved from website

Bedding, R. A., & Molyneux, A. S. (1982). Penetration of insect cuticle by infective juveniles of Heterorhabditis Spp. (Heterorhabditidae: Nematoda). Nematologica, 28(3), 354–359. DOI

Blatt, S. E., & Barry, S. (2020). Movement and infectivity of entomopathogenic nematodes in sandy loam soil from a carrot field in Nova Scotia: a laboratory study. Journal of the Acadian Entomological Society, 16, 1–6. Retrieved from PDF

Caamano, E. X., Cloyd, R. A., Solter, L. F., & Fallon, D. J. (2008). Quality assessment of two commercially available species of entomopathogenic nematodes: Steinernema feltiae and Heterorhabditis indica. HortTechnology, 18(1), 84–89. DOI

De Carvalho Barbosa Negrisoli, C. R., Negrisoli Júnior, A. S., Bernardi, D., & Garcia, M. S. (2013). Activity of eight strains of entomopathogenic nematodes (Rhabditida: Steinernematidae, Heterorhabditidae) against five stored product pests. Experimental Parasitology, 134(3), 384–388. DOI

Dowds, B. C. A., & Peters, A. (2002). Virulence mechanisms. In R. Gaugler (Ed.), Entomopathogenic nematology (pp. 79–98). Wallingford: CABI. Retrieved from website

Ehlers, R.-U. (2005). Forum on safety and regulation. In P. S. Grewal, R.-U. Ehlers, & Shapiro-Ilan, D. I. (Eds.), Nematodes as biocontrol agents (pp. 107–114). Wallingford: CAB International. Retrieved from website

Ehlers, R.-U., & Hokkanen, H. M. T. (1996). Insect biocontrol with non-endemic entomopathogenic nematodes (Steinernema and Heterorhabditis spp.): Conclusions and recommendations of a combined OECD and COST workshop on scientific and regulatory policy issues. Biocontrol Science and Technology, 6(3), 295–302. DOI

Eisfelder, C., Klein, I., Niklaus, M., & Kuenzer, C. (2014). Net primary productivity in Kazakhstan, its spatio-temporal patterns and relation to meteorological variables. Journal of Arid Environments, 103, 17–30. DOI

El Aalaoui, M., Mokrini, F., Dababat, A. A., Lahlali, R., & Sbaghi, M. (2022). Moroccan entomopathogenic nematodes as potential biocontrol agents against Dactylopius opuntiae (Hemiptera: Dactylopiidae). Scientific Reports, 12, 1–17. DOI

El Aimani, A., Houari, A., Laasli, S.-E., Mentag, R., Iraqi, D., Diria, G., … Mokrini, F. (2022). Antagonistic potential of Moroccan entomopathogenic nematodes against root-knot nematodes, Meloidogyne javanica on tomato under greenhouse conditions. Scientific Reports, 12, 1–9. DOI

Ensafi, P., Crowder, D. W., Esser, A. D., Zhao, Z., Marshall, J. M., & Rashed, A. (2018). Soil type mediates the effectiveness of biological control against Limonius californicus (Coleoptera: Elateridae). Journal of Economic Entomology, 111(5), 2053–2058. Retrieved from website

Fallet, P., De Gianni, L., Machado, R. A. R., Bruno, P., Bernal, J. S., Karangwa, P., … Turlings, T. C. J. (2022). Comparative screening of Mexican, Rwandan and commercial entomopathogenic nematodes to be used against invasive fall armyworm, Spodoptera frugiperda. Insects, 13(2), 205. DOI

FAO. (2021). World Food and Agriculture - Statistical Yearbook 2021. Rome, IT: FAO. DOI

Garriga, A., Morton, A., & Garcia-del-Pino, F. (2018). Is Drosophila suzukii as susceptible to entomopathogenic nematodes as Drosophila melanogaster? Journal of Pest Science, 91(2), 789–798. DOI

Jaffuel, G., Imperiali, N., Shelby, K., Campos-Herrera, R., Geisert, R., Maurhofer, M., … Hibbard, B. E. (2019). Protecting maize from rootworm damage with the combined application of arbuscular mycorrhizal fungi, Pseudomonas bacteria and entomopathogenic nematodes. Scientific Reports, 9(1), 3127. DOI

Jagodič, A., Trdan, S., & Laznik, Ž. (2019). Entomopathogenic nematodes: Can we use the current knowledge on belowground multitrophic interactions in future plant protection programmes? - Review. Plant Protection Science, 55(4), 243–254. DOI

James, M., Malan, A. P., & Addison, P. (2018). Surveying and screening South African entomopathogenic nematodes for the control of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann). Crop Protection, 105, 41–48. DOI

Javed, S., Khanum, T. A., & Khan, S. (2020). Biocontrol potential of entomopathogenic nematode species against Tribolium confusum (Jac.) (Coleoptera: Tenebrionidae) and Rhyzopertha dominica (Fab.) (Coleoptera: Bostrichidae) under laboratory conditions. Egyptian Journal of Biological Pest Control, 30, 5. DOI

Kerchev, I. A., Kryukova, N. A., Kryukov, V. Y., & Glupov, V. V. (2017). Entomoparasitic nematodes Sychnotylenchus sp. (Anguinidae) on the four-eyed fir bark beetle Polygraphus proximus: effects on the host's immunity and its susceptibility to Beauveria bassiana. Invertebrate Survival Journal, 14(1), 324-329. DOI

Koppenhöfer, A. M., Shapiro-Ilan, D. I., & Hiltpold, I. (2020). Entomopathogenic nematodes in sustainable food production. Frontiers in Sustainable Food Systems, 4, 1–14. DOI

Kuhar, T. P., Doughty, H. B., Speese III, J., & Reiter, S. (2008). Wireworm pest management in potatoes. Virginia Cooperative Extention. Virginia Polytechnic Institute and State University. Retrieved from website

Kusainova, A. A., Mezentseva, O. V., & Tusupbekov, Z. A. (2020). Influence of precipitation variability and temperature conditions on the yield of grain crops in Northern Kazakhstan. IOP Conference Series: Earth and Environmental Science, 548(4), 042026. DOI

Labaude, S., & Griffin, C. T. (2018). Transmission success of entomopathogenic nematodes used in pest control. Insects, 9(2), 72. DOI

Lacey, L. A., Grzywacz, D., Shapiro-Ilan, D. I., Frutos, R., Brownbridge, M., & Goettel, M. S. (2015). Insect pathogens as biological control agents: back to the future. Journal of Invertebrate Pathology, 132, 1–41. DOI

Lewis, E. E., & Clarke, D. J. (2012). Nematode parasites and entomopathogens. In F. Vega, & H. K. Kaya (Eds.), Insect Pathology (2nd ed.; pp. 395–424). Amsterdam, The Netherlands: Elsevier. Retrieved from website

Malan, A. P., & Moore, S. D. (2016). Evaluation of local entomopathogenic nematodes for the control of false codling moth, Thaumatotibia leucotreta (Meyrick, 1913), in a citrus orchard in South Africa. African Entomology, 24(2), 489–501. DOI

Matuska-łyżwa, J., Żarnowiec, P., & Kaca, W. (2021). Comparison of biological activity of field isolates of Steinernema feltiae with a commercial S. feltiae biopesticide product. Insects, 12(9), 816. DOI

Navarez, M. L., Sangcopan, R., Aryal, S., Sumaya, N. P. D., Bhat, A. H., & Sumaya, N. H. (2021). Native Philippine Heterorhabditis indica isolates from banana and rice fields and preliminary results of their virulence against the larvae of super worm (Zophobas morio Fabricius Coleoptera: Tenebrionidae). Egyptian Journal of Biological Pest Control, 31(1), 46. DOI

Neville, A. C. (1975). Biology of the arthropod cuticle. Springer. DOI

Öğretmen, A., Yüksel, E., & Canhilal, R. (2020). Susceptibility of larvae of wireworms (Agriotes spp.) (Coleoptera: Elateridae) to some Turkish isolates of entomopathogenic nematodes under laboratory and field conditions. Biological Control, 149, 104320. DOI

Peters, A., & Ehlers, R.-U. (1994). Susceptibility of leatherjackets (Tipula paludosa and Tipula oleracea; Tipulidae; Nematocera) to the entomopathogenic nematode Steinernema feltiae. Journal of Invertebrate Pathology, 63(2), 163–171. DOI

Platt, T., Stokwe, N. F., & Malan, A. P. (2018). Potential of local entomopathogenic nematodes for control of the vine mealybug, Planococcus ficus. South African Journal of Enology and Viticulture, 39(2), 1–8. DOI

Po, E., Sinha, N. K., & Naeem, S. (2018). Potato production, postharvest quality, and processed products. In M. Siddiq, & M. A. Uebersax (Eds.), Handbook of Vegetables and Vegetable Processing (2nd ed.; pp. 785-809). DOI

Propastin, P. A., Kappas, M., Erasmi, S., & Muratova, N. R. (2007). Remote sensing based study on intra-annual dynamics of vegetation and climate in drylands of Kazakhastan. Basic and Applied Dryland Research, 1(2), 138–154. DOI

Půža, V., Nermut’, J., Konopická, J., & Habuštová, O. S. (2021). Efficacy of the applied natural enemies on the survival of colorado potato beetle adults. Insects, 12(11), 1030. DOI

R Core Team. (2021). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Salnikov, V., Turulina, G., Polyakova, S., Petrova, Y., & Skakova, A. (2015). Climate change in Kazakhstan during the past 70 years. Quaternary International, 358, 77–82. DOI

Sandhi, R. K., Shapiro-Ilan, D., & Reddy, G. V. P. (2020). Montana native entomopathogenic nematode species against Limonius californicus (Coleoptera: Elateridae). Journal of Economic Entomology, 113(5), 2104–2111. DOI

Sandhi, R. K., Shapiro-Ilan, D., Sharma, A., & Reddy, G. V. P. (2020). Efficacy of entomopathogenic nematodes against the sugarbeet wireworm, Limonius californicus (Mannerheim) (Coleoptera: Elateridae). Biological Control, 143, 104190. DOI

Seal, D. R., Baniya, A. B., Dyrdahl-Young, R., Hochmuth, R. C., Leppla, N. C., Fenneman, D. K., … DiGennaro, P. (2020). Wireworm (Coleoptera: Elateridae) species composition and management in sweet potato grown in north Florida using chemical insecticides and entomopathogenic nematodes. Environmental Entomology, 49(6), 1415–1426. DOI

Shapiro-Ilan, D. I., & Brown, I. (2013). Earthworms as phoretic hosts for Steinernema carpocapsae and Beauveria bassiana: Implications for enhanced biological control. Biological Control, 66(1), 41–48. DOI

Shapiro-Ilan, D., Arthurs, S. P., & Lacey, L. A. (2017). Microbial control of arthropod pests of orchards in temperate climates. In Microbial Control of Insect and Mite Pests (pp. 253–267). Academic Press. DOI

Sharma, M. P., Sharma, A. N., & Hussaini, S. S. (2011). Entomopathogenic nematodes, a potential microbial biopesticide: Mass production and commercialisation status - a mini review. Archives of Phytopathology and Plant Protection, 44(9), 855–870. DOI

Stuart, R. J., Barbercheck, M. E., & Grewal, P. S. (2015). Entomopathogenic nematodes in the soil environment: distributions, interactions and the influence of biotic and abiotic factors. In R. Campos-Herrera (Ed.), Nematode pathogenesis of insects and other pests (pp. 97–137). DOI

Temreshev, I. I., Makezhanov, A. M., Yeszhanov, A. B., & Tursynkulov, A. M. (2020). Preliminary evaluation of the effectiveness of entomopathogenic nematodes Heterorabditis bacteriophora Poinar, 1975, Steinernema feltiae (Filipjev, 1934) and S. carpocapsae (Weiser, 1955) against the click beetle crusader Aeoloderma crucifer (Rossi, 1790) (Insecta, Coleoptera, Elateridae) on soybean crops in Southeast Kazakhstan. Izvestiâ Nacionalʹnoj Akademii Nauk Respubliki Kazahstan, 2(56), 70–77. Retrieved from website


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