ENTEGRE ZARARLI YÖNETİMİ STRATEJİLERİNDE ENTOMOPATOJEN NEMATODLARIN YERİ VE KULLANIM POTANSİYELİ
Özet
Tarımda Entegre Mücadele, zararlı popülasyonlarının ekonomik zarar düzeyinin altında tutulmasında biyolojik, kültürel, fiziksel, biyoteknik ve kimyasal mücadele yöntemlerinin birbirini tamamlayacak biçimde kullanılmasını esas alan sürdürülebilir bir yaklaşımdır. Entomopatojen nematodlar (EPN’ler), özellikle Steinernema ve Heterorhabditis cinslerine ait türler, sahip oldukları biyolojik ve ekolojik özellikler nedeniyle IPM programlarında önemli biyolojik mücadele ajanları arasında yer almaktadır. EPN’lerin etkinliği, Steinernema–Xenorhabdus ve Heterorhabditis–Photorhabdus birlikteliklerine dayanan özgün enfeksiyon mekanizması sayesinde hedef böceklerin kısa sürede öldürülmesi ve nematodların konukçu içerisinde çoğalmasıyla gerçekleşmektedir. Bununla birlikte, laboratuvar koşullarında belirlenen yüksek virülens her zaman başarılı bir saha uygulamasına dönüşmemektedir. EPN türü veya izolatının konukçu arama davranışı, hedef zararlının duyarlı yaşam dönemi ve bulunduğu mikrohabitat ile sıcaklık, nem, toprak özellikleri ve uygulama zamanının birbiriyle uyumlu olması saha başarısını belirleyen temel unsurlardır. EPN’ler özellikle toprakta yaşayan, pupalaşmak amacıyla toprağa geçen veya korunaklı mikrohabitatlarda bulunan Coleoptera, Lepidoptera ve Diptera türlerinin yönetiminde önemli kullanım potansiyeline sahiptir. Ayrıca kimyasal insektisitler, entomopatojen funguslar, bakteriyel biyopestisitler, predatörler, parazitoitler ve kültürel mücadele yöntemleriyle uygun biçimde bütünleştirilebilmeleri, bu biyolojik mücadele etmenlerinin entegre mücadele içerisindeki işlevsel değerini artırmaktadır. Günümüzde formülasyon teknolojileri, çevresel strese dayanıklı izolatların seçimi, hedefe yönelik uygulama sistemleri ve hassas tarım yaklaşımlarındaki gelişmeler EPN kullanımının etkinliğini ve ekonomik uygulanabilirliğini geliştirme potansiyeli taşımaktadır. Sonuç olarak EPN’ler, kimyasal insektisitlerin genel bir ikamesinden ziyade, doğru zararlı–yaşam dönemi–mikrohabitat eşleşmesi sağlandığında kimyasal girdilerin azaltılmasına ve sürdürülebilir zararlı yönetiminin geliştirilmesine katkı sağlayabilecek güçlü bir biyolojik mücadele aracıdır.
Anahtar Kelimeler: Entomopatojen nematodlar, entegre zararlı yönetimi, biyolojik mücadele, Steinernema, Heterorhabditis
Konu Alanı: Biyoloji -> Biyoloji (diğer) -> Entomoloji ve Parazitoloji
Acharya, R., Hwang, H.-S., Shim, J.-K., Yu, Y.-S., & Lee, K.-Y. (2019). Control efficacy of fungus gnat, Bradysia impatiens, enhanced by a combination of entomopathogenic nematodes and predatory mites. Biological Control, 138, 104071. https://doi.org/10.1016/j.biocontrol.2019.104071
Aioub, A. A. A., El-Ashry, R. M., Hashem, A. S., Elesawy, A. E., & Elsobki, A. E. A. (2021). Compatibility of entomopathogenic nematodes with insecticides against the cabbage white butterfly, Pieris rapae L. (Lepidoptera: Pieridae). Egyptian Journal of Biological Pest Control, 31, 153. https://doi.org/10.1186/s41938-021-00498-z
Alwaneen, W. S., Tahir, M., Avery, P. B., Wakil, W., Kavallieratos, N. G., Eleftheriadou, N., Boukouvala, M. C., Rasool, K. G., Husain, M., & Aldawood, A. S. (2024). Initial evaluation of the entomopathogenic fungi Beauveria bassiana and Metarhizium robertsii, and the entomopathogenic nematode Heterorhabditis bacteriophora, individually and in combination against the noxious Helicoverpa armigera (Lepidoptera: Noctuidae). Agronomy, 14(7), 1395. https://doi.org/10.3390/agronomy14071395
Amizadeh, M., Hejazi, M. J., Niknam, G., & Askari-Saryazdi, G. (2019). Interaction between the entomopathogenic nematode, Steinernema feltiae and selected chemical insecticides for management of the tomato leafminer, Tuta absoluta. BioControl, 64, 709–721. https://doi.org/10.1007/s10526-019-09973-x
Atwa, A. A., Hegazi, E. M., Khafagi, W. E., & Abd El-Aziz, G. M. (2013). Interaction of the koinobiont parasitoid Microplitis rufiventris of the cotton leafworm, Spodoptera littoralis, with two entomopathogenic rhabditids, Heterorhabditis bacteriophora and Steinernema carpocapsae. Journal of Insect Science, 13, 84. https://doi.org/10.1673/031.013.8401
Barzman, M., Bàrberi, P., Birch, A. N. E., Boonekamp, P. M., Dachbrodt-Saaydeh, S., Graf, B., Hommel, B., Jensen, J. E., Kiss, J., Kudsk, P., Lamichhane, J. R., Messéan, A., Moonen, A. C., Ratnadass, A., Ricci, P., Sarah, J. L., & Sattin, M. (2015). Eight principles of integrated pest management. Agronomy for Sustainable Development, 35(4), 1199–1215. https://doi.org/10.1007/s13593-015-0327-9
Buitenhuis, R., & 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(5), 1480–1485. https://doi.org/10.1093/jee/98.5.1480
Campbell, J. F., & Gaugler, R. R. (1997). Inter-specific variation in entomopathogenic nematode foraging strategy: Dichotomy or variation along a continuum? Fundamental and Applied Nematology, 20(4), 393–398.
Campbell, J. F., Lewis, E. E., Stock, S. P., Nadler, S., & Kaya, H. K. (2003). Evolution of host search strategies in entomopathogenic nematodes. Journal of Nematology, 35(2), 142–145.
Correa-Cuadros, J. P., Sáenz-Aponte, A., & Rodríguez-Bocanegra, M. X. (2016). In vitro interaction of Metarhizium anisopliae Ma9236 and Beauveria bassiana Bb9205 with Heterorhabditis bacteriophora HNI0100 for the control of Plutella xylostella. SpringerPlus, 5, 2068. https://doi.org/10.1186/s40064-016-3745-5
Dias, S. da C., de Brida, A. L., Jean-Baptiste, M. C., Leite, L. G., Ovruski, S. M., Lee, J. C., & Garcia, F. R. M. (2024). Compatibility of entomopathogenic nematodes with chemical insecticides for the control of Drosophila suzukii (Diptera: Drosophilidae). Plants, 13(5), 632. https://doi.org/10.3390/plants13050632
Ebssa, L., Borgemeister, C., & Poehling, H.-M. (2006). Simultaneous application of entomopathogenic nematodes and predatory mites to control western flower thrips Frankliniella occidentalis. Biological Control, 39(1), 66–74. https://doi.org/10.1016/j.biocontrol.2006.02.005
Ebssa, L., Borgemeister, C., Berndt, O., & 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(3), 119–127. https://doi.org/10.1006/jipa.2001.5051
Fallet, P., De Gianni, L., Machado, R. A. R., Bruno, P., Bernal, J. S., Karangwa, P., Kajuga, J., Waweru, B., Bazagwira, D., Degen, T., Toepfer, S., & 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. https://doi.org/10.3390/insects13020205
Fitters, P. F. L., Meijer, E. M. J., Wright, D. J., & Griffin, C. T. (1997). Estimation of lipid reserves in unstained living and dead nematodes by image analysis. Journal of Nematology, 29(2), 160–167.
Gang, S. S., & Hallem, E. A. (2016). Mechanisms of host seeking by parasitic nematodes. Molecular and Biochemical Parasitology, 208(1), 23–32. https://doi.org/10.1016/j.molbiopara.2016.05.007
Garriga, A., Morton, A., García-López, D., & García-del-Pino, F. (2019). Compatibility of entomopathogenic nematodes with natural enemies for horticultural pest control. Biological Control, 138, 104050. https://doi.org/10.1016/j.biocontrol.2019.104050
Gaugler, R. (Ed.). (2002). Entomopathogenic nematology. CABI Publishing.
Gaugler, R., Grewal, P. S., Kaya, H. K., & Smith-Fiola, D. (2000). Quality assessment of commercially produced entomopathogenic nematodes. Biological Control, 17(1), 100–109. https://doi.org/10.1006/bcon.1999.0768
Grewal, P. S., Lewis, E. E., Gaugler, R., & Campbell, J. F. (1994). Host finding behaviour as a predictor of foraging strategy in entomopathogenic nematodes. Parasitology, 108(2), 207–215.
Harris, M. A., Oetting, R. D., & Gardner, W. A. (1995). Use of entomopathogenic nematodes and a new monitoring technique for control of fungus gnats, Bradysia coprophila (Diptera: Sciaridae), in floriculture. Biological Control, 5(3), 412–418. https://doi.org/10.1006/bcon.1995.1049
Kapranas, A., Chronopoulou, A., Lytra, I. C., Peters, A., Milonas, P. G., & Papachristos, D. P. (2021). Efficacy and residual activity of commercially available entomopathogenic nematode strains for Mediterranean fruit fly control and their ability to infect infested fruits. Pest Management Science, 77(9), 3964–3969. https://doi.org/10.1002/ps.6416
Kaya, H. K., Burlando, T. M., Choo, H. Y., & Thurston, G. S. (1995). Integration of entomopathogenic nematodes with Bacillus thuringiensis or pesticidal soap for control of insect pests. Biological Control, 5(3), 432–441. https://doi.org/10.1006/bcon.1995.1052
Khan, R. R., Arshad, M., Aslam, A., & Arshad, M. (2021). Additive interactions of some reduced-risk biocides and two entomopathogenic nematodes suggest implications for integrated control of Spodoptera litura (Lepidoptera: Noctuidae). Scientific Reports, 11, 1268. https://doi.org/10.1038/s41598-020-79725-w
Koppenhöfer, A. M., & Kaya, H. K. (1997). Additive and synergistic interaction between entomopathogenic nematodes and Bacillus thuringiensis for scarab grub control. Biological Control, 8(2), 131–137. https://doi.org/10.1006/bcon.1996.0498
Koppenhöfer, A. M., Choo, H. Y., Kaya, H. K., Lee, D. W., & Gelernter, W. D. (1999). Increased field and greenhouse efficacy against scarab grubs with a combination of an entomopathogenic nematode and Bacillus thuringiensis. Biological Control, 14(1), 37–44. https://doi.org/10.1006/bcon.1998.0663
Koppenhöfer, A. M., & Grewal, P. S. (2005). Compatibility and interactions with agrochemicals and other biocontrol agents. In P. S. Grewal, R.-U. Ehlers, & D. I. Shapiro-Ilan (Eds.), Nematodes as biocontrol agents (pp. 363–381). CABI Publishing. https://doi.org/10.1079/9780851990170.0363
Koppenhöfer, A. M., & Fuzy, E. M. (2006). Effect of soil type on infectivity and persistence of the entomopathogenic nematodes Steinernema scarabaei, Steinernema glaseri, Heterorhabditis zealandica, and Heterorhabditis bacteriophora. Journal of Invertebrate Pathology, 92(1), 11–22. https://doi.org/10.1016/j.jip.2006.02.003
Koppenhöfer, A. M., & Fuzy, E. M. (2007). Soil moisture effects on infectivity and persistence of the entomopathogenic nematodes Steinernema scarabaei, S. glaseri, Heterorhabditis zealandica, and H. bacteriophora. Applied Soil Ecology, 35(1), 128–139. https://doi.org/10.1016/j.apsoil.2006.05.007
Koppenhöfer, A. M., & Foye, S. (2024). Interactions between agrochemicals and biological control agents. In D. I. Shapiro-Ilan & E. E. Lewis (Eds.), Entomopathogenic nematodes as biological control agents (pp. 494–518). CABI. https://doi.org/10.1079/9781800620322.0027
Kotliarevski, L., Cohen, R., Ramakrishnan, J., Wu, S., Mani, K. A., Amar-Feldbaum, R., & Mechrez, G. (2022). Individual coating of entomopathogenic nematodes with titania (TiO₂) nanoparticles based on oil-in-water Pickering emulsion: A new formulation for biopesticides. Journal of Agricultural and Food Chemistry, 70(42), 13518–13527. https://doi.org/10.1021/acs.jafc.2c04424
Kotsinis, V., Dritsoulas, A., Ntinokas, D., Bouga, M., & O. Giannakou, I. (2026). Pest control or pollinator peril? Evaluating entomopathogenic nematodes risks to Apis mellifera honey bees. Journal of Apicultural Research, 1-9.
Lacey, L. A., & Georgis, R. (2012). Entomopathogenic nematodes for control of insect pests above and below ground with comments on commercial production. Journal of Nematology, 44(2), 218–225.
Lewis, E. E., Campbell, J., Griffin, C., Kaya, H., & Peters, A. (2006). Behavioral ecology of entomopathogenic nematodes. Biological Control, 38(1), 66–79. https://doi.org/10.1016/j.biocontrol.2005.11.007
Maushe, D., Ogi, V., Divakaran, K., Verdecia Mogena, A. M., Himmighofen, P. A., Machado, R. A. R., Towbin, B. D., Ehlers, R.-U., Molina, C., Parisod, C., & Robert, C. A. M. (2023). Stress tolerance in entomopathogenic nematodes: Engineering superior nematodes for precision agriculture. Journal of Invertebrate Pathology, 199, 107953. https://doi.org/10.1016/j.jip.2023.107953
Millar, L. C., & Barbercheck, M. E. (2002). Effects of tillage practices on entomopathogenic nematodes in a corn agroecosystem. Biological Control, 25(1), 1–11. https://doi.org/10.1016/S1049-9644(02)00042-7
Moisan, K., Kostenko, O., Galeano, M., Soler, R., van der Ent, S., & Hiltpold, I. (2024). The sky is not the limit: Successful foliar application of Steinernema spp. entomopathogenic nematodes to control Lepidopteran caterpillars. Journal of Invertebrate Pathology, 206, 108163. https://doi.org/10.1016/j.jip.2024.108163
Mokrini, F., Laasli, S.-E., Benseddik, Y., Boutaleb Joutei, A., Blenzar, A., Lakhal, H., Sbaghi, M., Imren, M., Özer, G., Paulitz, T., Lahlali, R., & Dababat, A. A. (2020). Potential of Moroccan entomopathogenic nematodes for the control of the Mediterranean fruit fly Ceratitis capitata Wiedemann (Diptera: Tephritidae). Scientific Reports, 10, 19204. https://doi.org/10.1038/s41598-020-76170-7
Nishimatsu, T., & Jackson, J. J. (1998). Interaction of insecticides, entomopathogenic nematodes, and larvae of the western corn rootworm (Coleoptera: Chrysomelidae). Journal of Economic Entomology, 91(2), 410–418. https://doi.org/10.1093/jee/91.2.410
Oliveira-Hofman, C., Kaplan, F., Stevens, G., Lewis, E., Wu, S., Alborn, H. T., Perret-Gentil, A., & Shapiro-Ilan, D. I. (2019). Pheromone extracts act as boosters for entomopathogenic nematodes efficacy. Journal of Invertebrate Pathology, 164, 38–42. https://doi.org/10.1016/j.jip.2019.04.008
Patel, M. N., Stolinski, M., & Wright, D. J. (1997). Neutral lipids and the assessment of infectivity in entomopathogenic nematodes: Observations on four Steinernema species. Parasitology, 114(5), 489–496. https://doi.org/10.1017/S0031182096008748
Patil, J., Nekkanti, A., Gowda, M. T., Aravindaram, K., Subaharan, K., & Sushil, S. N. (2026). Entomopathogenic nematodes and fungi work synergistically to mitigate Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) in maize. Crop Protection, 207, 107672. https://doi.org/10.1016/j.cropro.2026.107672
Perier, J. D., Wu, S., Arthurs, S. P., Toews, M. D., & Shapiro-Ilan, D. I. (2025). Persistence of the entomopathogenic nematode Steinernema feltiae in a novel capsule formulation. Biological Control, 200, 105684. https://doi.org/10.1016/j.biocontrol.2024.105684
Piñero, J. C., Shapiro-Ilan, D., Cooley, D. R., Tuttle, A. F., Eaton, A., Drohan, P., Leahy, K., Zhang, A., Hancock, T., Wallingford, A. K., & Leskey, T. C. (2020). Toward the integration of an attract-and-kill approach with entomopathogenic nematodes to control multiple life stages of plum curculio (Coleoptera: Curculionidae). Insects, 11(6), 375. https://doi.org/10.3390/insects11060375
Půža, V., & Machado, R. A. R. (2024). Systematics and phylogeny of the entomopathogenic nematobacterial complexes Steinernema–Xenorhabdus and Heterorhabditis–Photorhabdus. Zoological Letters, 10, 13. https://doi.org/10.1186/s40851-024-00235-y
Půža, V., & Tarasco, E. (2023). Interactions between entomopathogenic fungi and entomopathogenic nematodes. Microorganisms, 11(1), 163. https://doi.org/10.3390/microorganisms11010163
Ramakuwela, T., Tarasco, E., Chavarría-Hernández, N., & Toepfer, S. (2025). Entomopathogenic nematodes: Commercial use and future perspectives. Journal of Invertebrate Pathology, 212, 108388. https://doi.org/10.1016/j.jip.2025.108388
Rasmann, S., Köllner, T. G., Degenhardt, J., Hiltpold, I., Toepfer, S., Kuhlmann, U., Gershenzon, J., & Turlings, T. C. J. (2005). Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature, 434, 732–737. https://doi.org/10.1038/nature03451
Shapiro-Ilan, D. I., Gouge, D. H., Piggott, S. J., & Fife, J. P. (2006). Application technology and environmental considerations for use of entomopathogenic nematodes in biological control. Biological Control, 38(1), 124–133. https://doi.org/10.1016/j.biocontrol.2005.09.005
Shapiro-Ilan, D. I., Han, R., & Dolinski, C. (2012). Entomopathogenic nematode production and application technology. Journal of Nematology, 44(2), 206–217.
Shapiro-Ilan, D. I., Hazir, S., & Glazer, I. (2017). Basic and applied research: Entomopathogenic nematodes. In L. A. Lacey (Ed.), Microbial control of insect and mite pests: From theory to practice (pp. 91–105). Academic Press. https://doi.org/10.1016/B978-0-12-803527-6.00006-8
Shapiro-Ilan, D. I., & Lewis, E. E. (2024). Formulation and application technology for entomopathogenic nematodes. In D. I. Shapiro-Ilan & E. E. Lewis (Eds.), Entomopathogenic nematodes as biological control agents (pp. 201–218). CABI. https://doi.org/10.1079/9781800620322.0011
Shapiro-Ilan, D. I., Ment, D., Ramakrishnan, J., Rodríguez Hernández, M. G., & Duncan, L. W. (2025). A century of advancement in entomopathogenic nematode formulation and application technology. Journal of Invertebrate Pathology, 212, 108389. https://doi.org/10.1016/j.jip.2025.108389
Shaurub, E. H. (2023). Review of entomopathogenic fungi and nematodes as biological control agents of tephritid fruit flies: Current status and a future vision. Entomologia Experimentalis et Applicata, 171(1), 17–34. https://doi.org/10.1111/eea.13244
Terzioğlu, A., Aksu, R. N., Ulu, T. C., & Zelyüt, F. R. (2025). Characterization of native entomopathogenic nematode isolates from Bilecik, Türkiye: Heat tolerance, dispersal, and pathogenicity. European Journal of Life Sciences, 4(2), 55–63. https://doi.org/10.55971/EJLS.1696030
Van Damme, V. M., Beck, B. K. E. G., Berckmoes, E., Moerkens, R., Wittemans, L., De Vis, R., Nuyttens, D., Casteels, H. F., Maes, M., Tirry, L., & De Clercq, P. (2016). Efficacy of entomopathogenic nematodes against larvae of Tuta absoluta in the laboratory. Pest Management Science, 72(9), 1702–1709. https://doi.org/10.1002/ps.4195
Yang, H., Jian, H., Zhang, S., & Zhang, G. (1997). Quality of the entomopathogenic nematode Steinernema carpocapsae produced on different media. Biological Control, 10(3), 193–198. https://doi.org/10.1006/bcon.1997.0557
ÇAKMAK, T. (2026). ENTEGRE ZARARLI YÖNETİMİ STRATEJİLERİNDE ENTOMOPATOJEN NEMATODLARIN YERİ VE KULLANIM POTANSİYELİ. In KARADAĞ, A. A. & DEMİROĞLU, D. (Eds.), TÜRKİYE TARIMININ 21. YÜZYIL YOLCULUĞU Cilt 1: Sürdürülebilir Üretim, Biyoteknoloji ve Bitki Sağlığı Türkiye’s Agricultural Journey in the 21st Century Volume 1: Sustainable Production, Biotechnology, and Plant Health (pp. -). Vizetek Yayıncılık. https://doi.org/10.54637/vizetek.9786253824334
| Kitap: |
| Yayınevi:
Vizetek Yayıncılık |