Bazı Steinernema feltiae (Filipjev, 1934) (Rhabditida: Steinernematidae) izolatlarının Cryptolestes ferrugineus (Stephens, 1831) (Coleoptera: Laemophloeidae) üzerindeki ölüm oranı ve penetrasyon etkisinin değerlendirilmesi

Öz

Küçük kırma biti, Cryptolestes ferrugineus (Stephens, 1831) (Coleoptera: Laemophloeidae) depolanmış ürün ortamlarında ciddi zarara neden olan bir zararlıdır. Bu çalışmada, entomopatojen nematod Steinernema feltiae (Filipjev, 1934) (Rhabditida: Steinernematidae)’nin iki Türk izolatının ST6 ve TUR-S3'ün laboratuvar koşullarında ergin C. ferrugineus'a karşı insektisidal etkinliği değerlendirilmiştir. İnfektif juveniller (IJ'ler) beş konsantrasyon (50, 100, 150, 200 ve 250 IJs / Petri kabı) olarak uygulandı ve hem ölüm oranları hem de nematod penetrasyon seviyeleri belirlendi. Bu çalışma 2025 yılında Bursa Uludağ Üniversitesi, Bitki Koruma Bölümü, Nematoloji Laboratuvarında gerçekleştirilmiştir. Sonuçlar, her iki izolat için de ölüm oranında doza bağlı net bir artış olduğunu, TUR-S3'ün 250 IJ'de en yüksek ölüm oranına (%93,33) ulaştığını, bunu ST6'nın (%86,67) izlediğini ortaya koymuştur. Penetrasyon oranları da konsantrasyonla önemli ölçüde artarak, penetrasyon ile ölüm oranı arasında güçlü bir pozitif korelasyon olduğunu desteklemektedir (ST6 için r=0.8113; TUR-S3 için r=0.8850). İkisi arasında TUR-S3 sürekli olarak üstün performans sergilemiş ve daha yüksek penetrasyon ve enfeksiyon etkinliği elde etmiştir. Bu Türk S. feltiae izolatlarının C. ferrugineus'a karşı patojenitesini gösteren ilk rapordur ve sürdürülebilir hasat sonrası zararlı yönetimi stratejilerine entegre edilmeleri için çevre dostu biyolojik kontrol ajanları olarak potansiyellerini vurgulamaktadır.

Anahtar Kelimeler

• Biyolojik mücadele
• entomopatojen nematod
• patojenite
• penetrasyon
• depolanmış ürün zararlısı

Evaluating the impact of some Steinernema feltiae (Filipjev, 1934) (Rhabditida: Steinernematidae) isolates on Cryptolestes ferrugineus (Stephens, 1831) (Coleoptera: Laemophloeidae) mortality and penetration

Abstract

The rusty grain beetle, Cryptolestes ferrugineus (Stephens, 1831) (Coleoptera: Laemophloeidae) is a destructive pest in stored-product environments. This study evaluated the insecticidal efficacy of two Turkish isolates of the entomopathogenic nematode Steinernema feltiae (Filipjev, 1934) (Rhabditida: Steinernematidae) ST6 and TUR-S3-against adult C. ferrugineus under laboratory conditions in 2025 at the Nematology Laboratory of the Department of Plant Protection, Bursa Uludağ University. Infective juveniles (IJs) were applied at five concentrations (50, 100, 150, 200 and 250 IJs per petri dish), and both mortality rates and nematode penetration levels were recorded. Results revealed a clear dose-dependent increase in mortality for both isolates, with TUR-S3 achieving the highest mortality (93.33%) at 250 IJs, followed by ST6 (86.67%). Penetration rates also increased significantly with concentration, supporting a strong positive correlation between penetration and mortality (r=0.8113 for ST6; r=0.8850 for TUR-S3). Among the two, TUR-S3 consistently exhibited superior performance, obtaining higher virulence and infection efficiency. This is the first report demonstrating the pathogenicity of Turkish S. feltiae isolates against C. ferrugineus, underscoring their potential as eco-friendly biocontrol agents for integration into sustainable post-harvest pest management strategies.

Keywords

• Biocontrol
• entomopathogenic nematode
• pathogenicity
• penetration
• stored-product pest

Kaynakça

1. Abd El-Aziz, S. E., 2011. Control strategies of stored product pests. Journal of Entomology, 8 (2): 101-122.
2. Ali, S., M. I. Ullah, A. Sajjad, Q. Shakeel & A. Hussain, 2021. “Environmental and Health Effects of Pesticide Residues, 311-336”. Sustainable Agriculture Reviews 48 Pesticide Occurrence, Analysis and Remediation Vol. 2 Analysis (Eds. Inamuddin, M. I. Ahamed & E. Lichtfouse). Springer Cham International Publishing, 354 pp.
3. Angon, P. B., S. Mondal, I. Jahan, M. Datto, U. B. Antu, F. J. Ayshi & M. S. Islam, 2023. Integrated pest management (IPM) in agriculture and its role in maintaining ecological balance and biodiversity. Advances in Agriculture, 2023 (1): 5546373 (1-19).
4. Ayilara, M. S., B. S. Adeleke, S. A. Akinola, C. A. Fayose, U. T. Adeyemi, L. A. Gbadegesin, R. K. Omole, R. M. Jhonson, Q. O. Uthman & O. O. Babalola, 2023. Biopesticides as a promising alternative to synthetic pesticides: A case for microbial pesticides, phytopesticides, and nanobiopesticides. Frontiers in Microbiology, 14 (2023): 1040901 (1-16).
5. Bastidas, B., E. Portillo & E. San-Blas, 2014. Size does matter: the life cycle of Steinernema spp. in micro-insect hosts. Journal of Invertebrate Pathology, 121 (2014): 46-55.
6. Bharathi, V. S. K., F. Jian, D. S. Jayas & J. Morrison, 2022a. Three-dimensional movement and distribution of Cryptolestes ferrugineus (Coleoptera: Laemophloeidae) adults in stored wheat under constant temperatures and moisture contents. Environmental Entomology, 51 (1): 11-21.
7. Bharathi, V. S. K., D. S. Jayas & F. Jian, 2022b. Effects of insect density, movement period, and temperature on three-dimensional movement and distribution of adult Cryptolestes ferrugineus (Coleoptera: Laemophloeidae). Journal of Insect Science, 22 (3): 3 (1-9).
8. Bharathi, V. S. K., F. Jian & D. S. Jayas, 2023. Biology, Ecology, and Behavior of Rusty Grain Beetle (Cryptolestes ferrugineus (Stephens)). Insects, 14 (7): 590 (1-28).

9. Bist, N. S. & P. Bist, 2020. Role of microorganisms in post-harvest loss of agricultural products: A review. Sustainability in Food and Agriculture, 2 (1): 1-4.
10. Bütüner, A. K. & İ. A. Susurluk, 2023. Pathogenicity of Turkish entomopathogenic nematodes, Steinernema feltiae and Steinernema carpocapsae (Rhabditida: Steinernematidae) on the rice weevil: Sitophilus oryzae (Coleoptera: Curculionidae). Turkish Journal of Agricultural and Natural Sciences, 10 (3): 541-547.
11. Bütüner, A. K., E. Ergene, M. İlktan, S. Sepin, H. Susurluk & İ. A. Susurluk, 2024. Impact of some entomopathogenic nematode isolates on the mortality and penetration rate of Rhyzopertha dominica and Tenebrio molitor. Crop Protection, 179 (2024): 106629 (1-9).
12. Canhilal, R. & E. Yüksel, 2020. Laboratory evaluation of some native isolates of Steinernema feltiae against the Rice weevil, Sitophilus oryzae (L.) (Curculionidae: Coleoptera). Türkiye Biyolojik Mücadele Dergisi, 11 (1): 65-69.
13. Caroli, L., I. Glazer & R. Gaugler, 1996. Entomopathogenic nematode infectivity assay: comparison of penetration rate into different hosts. Biocontrol Science and Technology, 6 (2): 227-233.
14. Chèze, B., M. David & V. Martinet, 2020. Understanding farmers' reluctance to reduce pesticide use: A choice experiment. Ecological Economics, 167 (2020): 106349 (1-14).
15. Devi, G., 2022. Bioefficacy of insecticidal nematodes against stored grain pests: An overview. International Journal of Plant Soil Science, 34 (22): 532-536.
16. Ehlers, R. U., 2001. Mass production of entomopathogenic nematodes for plant protection. Applied Microbiology and Biotechnology, 56 (5-6): 623-633.
17. Flinn, P. W. & D. W. Hagstrum, 1998. Distribution of Cryptolestes ferrugineus (Coleoptera: Cucujidae) in response to temperature gradients in stored wheat. Journal of Stored Products Research, 34 (2-3): 107-112.
18. Forst, S. & K. Nealson, 1996. Molecular biology of the symbiotic-pathogenic bacteria Xenorhabdus spp. and Photorhabdus spp. Microbiology Reviews, 60 (1): 21-43.
19. Gaugler, R., E. Lewis & R. J. Stuart, 1997. Ecology in the service of biological control: the case of entomopathogenic nematodes. Oecologia, 109 (4): 483-489.
20. Griffin, C. T., N. E. Boemare & E. E. Lewis, 2005. “Biology and Behaviour, 47-64”. In: Nematodes as Biocontrol Agents (Eds. P. S. Grewal, R. U. Ehlers & D. I. Shapiro-Ilan). Wallingford, UK: CABI Publishing, 505 pp.
21. Hamilton, D., Á. Ambrus, R. Dieterle, A. Felsot, C. Harris, B. Petersen, K. Racke, S-S Wong, R. Gonzalez, K. Tanaka, M. Earl, G. Roberts & R. Bhula, 2004. Pesticide residues in food-acute dietary exposure. Pest Management Science: formerly Pesticide Science, 60 (4): 311-339.
22. Hertel, T. W., 2011. The global supply and demand for agricultural land in 2050: a perfect storm in the making? American Journal of Agricultural Economics, 93 (2): 259-275.
23. Heve, W. K., F. E. El-Borai, D. Carrillo & L. W. Duncan, 2018. Increasing entomopathogenic nematode biodiversity reduces efficacy against the Caribbean fruit fly Anastrepha suspensa: interaction with the parasitoid Diachasmimorpha longicaudata. Journal of Pest Science, 91 (2): 799-813.
24. Hossain, L., R. Rahman & M. S. Khan, 2017. “Alternatives of Pesticides, 147-165”. In: Pesticide Residue in Foods: Sources, Management, and Control (Eds. M. S. Khan & M. S. Rahman). Springer Cham International Publishing, 200 pp.
25. Jagadeesan, R., M. K. Nayak, K. Dawson, V. Byrne, P. J. Collins, 2013. Dietary media for mass rearing of rusty grain beetle, Cryptolestes ferrugineus (Stephens) and flat grain beetle, Cryptolestes pusillus (Schonherr)(Coleoptera: Cucujidae). Journal of Stored Products Research, 55: 68-72.
26. Javed, S., T. A. Khanum & S. Khan, 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 (1): 5 (1-6).
27. Kallali, N. S., M. El Jarroudi, J. Kenfaoui, Y. Benseddik, F. Mokrini, A. Ouijja, S-E Laasli, K. Goura, R. Lahlali, A. Blenzar, A. B. Joutei, M. E. Jarroudi, F. Mokrini & R. Lahlali, 2024. From soil to host: Discovering the tripartite interactions between entomopathogenic nematodes, symbiotic bacteria and insect pests and related challenges. Journal of Natural Pesticide Research, 7 (2024): 100065 (1-22).
28. Kar, D. & S. B. Dhal, 2025. Advancing food security through drone-based hyperspectral imaging: applications in precision agriculture and post-harvest management. Environmental Monitoring and Assessment, 197 (3): 283 (1-26).
29. Karanastasi, E., A. Nikorezou, M. Stamouli, A. Skourti, M. C. Boukouvala & N. G. Kavallieratos, 2025. Temperature effect on the efficacy of 3 entomopathogenic nematode isolates against larvae of the lesser mealworm, Alphitobius diaperinus (Coleoptera: Tenebrionidae). Journal of Economic Entomology, 118 (1): 93-99.
30. Karunakar, G., S. Easwaramoorthy & H. David, 2002. Interaction between entomopathogenic nematodes and granulosis viruses of Chilo infuscatellus Snellen and Chilo sacchariphagus indicus (Kapur). Journal of Biological Control, 16 (2): 153-156.
31. Kary, N. E., Z. Sanatipour, D. Mohammadi & G. Dunphy, 2022. Virulence and sex-dependent invasion efficiency of entomopathogenic nematodes on developmental stages of Phthorimaea operculella (Lep., Gelechidae). Journal of Asia-Pacific Entomology, 25 (1): 101874 (1-8).
32. Kavallieratos, N. G., E. Karanastasi, E. P. Nika, A. Skourti, M. C. Boukouvala & I. E. Sampazioti, 2022. Sustainable grain protectants: recruiting entomopathogenic nematodes against stored-product Coleopterans. Sustainability, 14 (23): 16038 (1-10).
33. Kaya, H. K. & R. Gaugler, 1993. Entomopathogenic nematodes. Annual Review of Entomology, 38: 181-206.
34. Kaya, H. K. & S. P. Stock, 1997. “Techniques in Insect Nematology, 281-324”. In: Manual of Techniques in Insect Pathology (Eds. L. A. Lacey). Academic Press, 409 pp.
35. Keating, B. A., M. Herrero, P. S. Carberry, J. Gardner & M. B. Cole, 2014. Food wedges: framing the global food demand and supply challenge towards 2050. Global Food Security, 3 (3-4): 125-132.
36. Kiaya, V., 2014. Post-harvest losses and strategies to reduce them. Technical Paper on Postharvest Losses, Action Contre la Faim (ACF), 25 (3): 1-25.
37. Koppenhöfer, A. M., P. S. Grewal & E. M. Fuzy, 2007. Differences in penetration routes and establishment rates of four entomopathogenic nematode species into four white grub species. Journal of Invertebrate Pathology, 94 (3): 184-195.
38. Kung, S. P., R. Gaugler & H. K. Kaya, 1991. Effects of soil temperature, moisture, and relative humidity on entomopathogenic nematode persistence. Journal of Invertebrate Pathology, 57 (2): 242-249.
39. Lalramnghaki, H. C., H. T. Lalremsanga, Vanramliana, Lalramliana, Vanlalhlimpuia & S. Lalliansanga, 2020. Evaluation of pathogenicity of indigenous entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) from Mizoram, India, against tobacco cutworm, Spodoptera litura (Fabricius, 1775). Journal of Environmental Biology, 41 (4 Special Issue): 851-860.
40. Laznik, Ž., T. Tóth, T. Lakatos, M. Vidrih & S. Trdan, 2010. Control of the Colorado potato beetle (Leptinotarsa decemlineata [Say]) on potato under field conditions: a comparison of the efficacy of foliar application of two strains of Steinernema feltiae (Filipjev) and spraying with thiametoxam. Journal of Plant Diseases and Protection, 117 (3): 129-135.
41. Leip, D., E. Rovenskaya & M. Wildemeersch, 2024. Risk-adjusted decision making can help protect food supply and farmer livelihoods in West Africa. Communications Earth & Environment, 5 (1): 101 (1-13).
42. Lewis, E. E., J. Campbell, C. Griffin, H. Kaya & A. Peters, 2006. Behavioral ecology of entomopathogenic nematodes. Biological Control, 38 (1): 66-79.
43. Liu, Z., A. Lv & T. Li, 2024. Intensified drought threatens future food security in major food-producing countries. Atmosphere, 16 (1): 34 (1-15).
44. Mahmood, I., S. R. Imadi, K. Shazadi, A. Gul & K. R. Hakeem, 2016. “Effects of Pesticides on Environment, 253-269”. In: Plant, Soil and Microbes: Volume 1: Implications in Crop Science (Eds. K. R. Hakeem, M. S. Akhtar & S. N. A. Abdullah). Springer International Publishing Switzerland, 366 pp.
45. Mahmood, M. H., M. Sultan & T. Miyazaki, 2019. Significance of temperature and humidity control for agricultural products storage: overview of conventional and advanced options. International Journal of Food Engineering, 15 (10): 20190063 (1-21).
46. Manickavasagan, A., D. S. Jayas & N. D. G. White, 2008. Thermal imaging to detect infestation by Cryptolestes ferrugineus inside wheat kernels. Journal of Stored Products Research, 44 (2): 186-192.
47. Mbata, G. N., C. Ivey & D. Shapiro-Ilan, 2018. The potential for using entomopathogenic nematodes and fungi in the management of the maize weevil, Sitophilus zeamais (Motschulsky) (Coleoptera: Curculionidae). Biological Control, 125: 39-43.
48. Reid, J. A., 1942. The relative sizes of different parts in beetle of the genus Laemophloeus (Coleopt.: Cucujidae). In: Proceedings of the Royal Entomological Society of London. Series A, General Entomology, 17 (1-3): 19-26.
49. Rumbos, C. I. & C. G. Athanassiou, 2017. The use of entomopathogenic nematodes in the control of stored-product insects. Journal of Pest Science, 90 (1): 39-49.
50. Said, P. P. & C. R. Pradhan, 2014. Food grain storage practices: A review. Journal of Grain Processing and Storage, 1 (1): 1-5.
51. Shah, B. P. & B. Devkota, 2009. Obsolete pesticides: their environmental and human health hazards. Journal of Agriculture and Environment, 10 (2009): 60-66.
52. Shahina, F. & J. Salma, 2010. Laboratory evaluation of seven Pakistani strains of entomopathogenic nematode against stored grain insect pest Sitophilus oryzae L. Pakistan Journal of Nematology, 28 (2): 295-305.
53. Shapiro-Ilan, D. I., D. H. Gouge, S. J. Piggott & J. P. Fife, 2006. Application technology and environmental considerations for use of entomopathogenic nematodes in biological control. Biological Control, 38 (1): 124-133.
54. Son, D. J., G. G. Kim, H. Y. Choo, H. J. Chung & Y. M. Choo, 2024. Functional comparison of three chitinases from symbiotic bacteria of entomopathogenic nematodes. Toxins, 16 (1): 26 (1-18).
55. Stathas, I. G., A. C. Sakellaridis, M. Papadelli, J. Kapolos, K. Papadimitriou & G. J. Stathas, 2023. The effects of insect infestation on stored agricultural products and the quality of food. Foods, 12 (10): 2046 (1-11).
56. Susurluk, A. & R. U. Ehlers, 2008. Field persistence of the entomopathogenic nematode Heterorhabditis bacteriophora in different crops. BioControl, 53 (4): 627-641.
57. Susurluk, H. & A. K. Bütüner, 2024. Effects of a native diatomaceous earth on Oryzaephilus surinamensis (L., 1758) (Coleoptera: Silvanidae), and Acanthoscelides obtectus (Say, 1831) (Coleoptera: Chrysomelidae). Harran Tarım ve Gıda Bilimleri Dergisi, 28 (1): 49-59.
58. Susurluk, H., A. K. Bütüner, E. Ergene, O. N. Yaraşır & İ. A. Susurluk, 2024. Is there any relationship between the effectiveness of some Heterorhabditis bacteriophora isolates on the host and their average penetration rate? Journal of Stored Products Research, 108 (2024): 102401 (1-6).
59. Toews, M. D. & T. W. Phillips, 2002. Factors affecting capture of Cryptolestes ferrugineus (Coleoptera: Laemophloeidae) in traps placed in stored wheat. Journal of economic entomology, 95 (1): 200-207.
60. Toews, M. D., T. W. Phillips & D. Shuman, 2003. Electronic and manual monitoring of Cryptolestes ferrugineus (Coleoptera: Laemophloeidae) in stored wheat. Journal of Stored Products Research, 39 (5): 541-554.
61. Trdan, S., M. Vidrih & N. Valič, 2006. Activity of four entomopathogenic nematode species against young adults of Sitophilus granarius (Coleoptera: Curculionidae) and Oryzaephilus surinamensis (Coleoptera: Silvanidae) under laboratory conditions. Journal of Plant Diseases and Protection, 113 (4): 168-173.
62. Tulek, A., S. Ertürk, I. Kepenekci & T. Atay, 2015. Efficacy of native entomopathogenic nematodes against the stored grain insect pest, Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae) adults. Egyptian Journal of Biological Pest Control, 25 (1): 251-254.
63. Ulu, T. C. & I. A. Susurluk, 2014. Heat and desiccation tolerances of Heterorhabditis bacteriophora strains and relationships between their tolerances and some bioecological characteristics. Invertebrate Survival Journal, 11 (1): 4-10.
64. Wakil, W., N. G. Kavallieratos, N. Eleftheriadou, T. Yaseen, K. G. Rasool, M. Husain & A. S. Aldawood, 2023. Natural warriors against stored-grain pests: the joint action of Beauveria bassiana and Steinernema carpocapsae. Journal of Fungi, 9 (8): 835 (1-15).
65. Xu, C., P. De Clercq, M. Moens, S. Chen & R. Han, 2010. Efficacy of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) against the striped flea beetle, Phyllotreta striolata. BioControl, 55 (6): 789-797.
66. Yağcı, M., F. Dolunay Erdoğuş, T. Akdeniz Fırat & S. Ertürk, 2022. Pathogenicity of four native isolates of entomopathogenic nematodes against Tribolium confusum Jacquelin du Val (Coleoptera: Tenebrionidae). Journal of Plant Diseases and Protection, 130 (1): 85-92.
67. Yaraşır, O. N., A. K. Bütüner & H. Susurluk 2024a. Recent advances on the potential control of Rhyzopertha dominica Fab. (Coleoptera: Bostrichidae). Bursa Uludağ Üniversitesi Ziraat Fakültesi Dergisi, 38 (2): 449-456.
68. Yaraşır, O. N., E. Ergene, A. K. Bütüner, H. Susurluk & A. Susurluk, 2024b. Pathogenicity of the Steinernema feltiae TUR-S3 (Rhabditida: Steinernematidae) isolate on Oryzaephilus surinamensis (Coleoptera: Silvanidae) and Tribolium confusum (Coleoptera: Tenebrionidae). Turkish Journal of Agricultural and Natural Sciences, 11 (2): 409-416.
69. Zhao, L., Q. Yu, M. Li, Y. Wang, G. Li, S. Sun, J. Fan & Y. Liu, 2022. A review of the innovative application of phase change materials to cold-chain logistics for agricultural product storage. Journal of Molecular Liquids, 365 (2022): 120088 (1-12).