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برهم‌کنش بین جدایه بومی نماتد بیماری‌زای حشرات، Steinernema carpocapsae IRMoghan 1 و حشره‌کش متافلومیزن در کنترل لاروهای مینوز برگ گوجه فرنگی Phthorimaea (=Tuta) absoluta (Meyrick) (Lepidoptera: Gelechiidae)

نوع مقاله : مقاله پژوهشی

نویسندگان

1 بخش تحقیقات کنترل بیولوژیک، موسسه تحقیقات گیاهپزشکی، سازمان تحقیقات، ترویج و آموزش کشاورزی، تهران، ایران.

2 بخش تحقیقات حشره شناسی موسسه گیاهپزشکی کشور، تهران، ایران

10.22059/ijpps.2026.411628.1007116

چکیده

کنترل شیمیایی معمولا روش اصلی برای کاهش خسارت مینوز برگ گوجه فرنگی Phthorimaea absoluta (Lepidoptera: Gelechiidae) است. با این حال، استفاده از روش‌های کنترل جایگزین ضروری می‌باشد. در این مطالعه، تاثیر جدایه بومی نماتد بیماری‌زای حشرات، Steinernema carpocapsae IRMoghan1، متافلومیزون و استفاده همزمان آنها علیه لاروهای P. absoluta داخل دالان لاروی برگ مورد ارزیابی قرار گرفت. در آزمایشی جداگانه تاثیر حشره‌کش روی زنده‌مانی نماتد بررسی شد. براساس نتایج، غلظت ۱۰۰۰ پی‌پی‌ام حشره‌کش به تنهایی (3/98 درصد) و نماتد به تنهایی (۹۵ درصد) بیشترین و غلظت‌ ۲۵۰ پی‌پی‌ام حشره‌کش (5/52 درصد)کمترین مرگ‌ومیر را ایجاد نمود. ترکیب نماتد و متافلومیزون ۸۵ درصد مرگ‌و‌میر آفت را در پی داشت که پارامترهای مورد ارزیابی نشان دهنده برهم‌کنش آنتاگونیستی بین نماتد و متافلومیزون بود. نتایج آزمایش سازگاری، مرگ‌ومیر 28/24 درصد لاروهای آلوده‌کننده نماتد با ۷۲ ساعت قرار گرفتن در معرض حشره‌کش را نشان داد. براساس گروه‌بندی IOBC/WPRS، متافلومیزون نسبت به این جدایه نماتد بی‌ضرر و سازگار بوده و در گروه یک قرار گرفت. درصد بالای مرگ‌ومیر در تیمار S. carpocapsae IRMoghan1 نشان دهنده توانایی این نماتد در عمل کردن به عنوان یک جستجوگر cruiser و آلوده کردن لاروهای حشره در داخل دالان لاروی است. یکی از دلایل برهم‌کنش آنتاگونیستی نماتد و متافلومیزون علیرغم قرار گرفتن این حشره‌کش در گروه بی‌ضرر و سازگار نسبت به این جدایه نماتد، درصد بالای مرگ و میر لاروهای آفت ناشی از نماتد به تنهایی است که پتانسیل مشاهده اثرات افزایشی و هم‌افزایی در تیمار ترکیبی را محدود کرده است. با این حال، دلایل کاهش کارایی نماتد نیازمند بررسی‌های بیشتر می‌باشد.

کلیدواژه‌ها


عنوان مقاله [English]

Interaction between the native entomopathogenic nematode isolate Steinernema carpocapsae IRMoghan1 and the insecticide metaflumizone in the control of the tomato leafminer, Phthorimaea (=Tuta) absoluta (Lepidoptera: Gelechiidae) larvae

نویسندگان [English]

  • Laleh Ebrahimi 1
  • Aziz SheikhiGarjan 2
1 Biological Control Research Department, Iranian Research Institute of Plant Protection, Agricultural Research, Education and Extension Organization (AREEO), Tehran, Iran,
2 Iranian Research Institute of Plant Protection, Agricultural Research, Education and Extension Organization (AREEO), Tehran, Iran.
چکیده [English]

Chemical control is generally the primary strategy to reduce damage caused by the tomato leaf miner, Phthorimaea absoluta (Lepidoptera: Gelechiidae). However, the implementation of alternative control approaches is essential. In the present study, the efficacy of the native entomopathogenic nematode isolate Steinernema carpocapsae IRMoghan1, metaflumizone, and their combined application was evaluated against larvae of P. absoluta within leaf mines. In a separate experiment, the effect of the insecticide on nematode survival was also assessed. According to the results, application of metaflumizone at 1000 ppm (98.3%) and the nematode alone (95%) resulted in the highest larval mortality, whereas the lowest mortality (52.5%) was observed at 250 ppm of metaflumizone. The combined application resulted in 86.7% pest mortality. Interaction analyses indicated an antagonistic interaction between the nematode and metaflumizone. Based on the compatibility assay, 24.28% mortality of infective juveniles was recorded after 72 h of exposure to the insecticide. According to IOBC/WPRS classification criteria, metaflumizone was categorized as harmless (Class 1) and compatible with S. carpocapsae IRMoghan1. The high mortality observed in the nematode treatment demonstrates its capacity to function effectively as a cruiser-type forager and to infect host larvae within leaf mines. One possible explanation for the observed antagonistic interaction, despite the classification of metaflumizone as harmless and compatible, is the already high level of mortality caused by the nematode alone, which may have limited the additive or synergistic effects in the combined treatment. Nevertheless, the underlying causes of the reduced efficacy of the nematode in combination treatments warrant further investigation.

کلیدواژه‌ها [English]

  • antagonistic
  • compatibility
  • foraging strategy
  • native isolate

Extended Abstract

Introduction

    The tomato leafminer, Phthorimaea absoluta (Lepidoptera: Gelechiidae), is one of the most economically important pests of tomato crops in both open-field and greenhouse production systems. The entomopathogenic nematode Steinernema carpocapsae is among the most commercially utilized entomopathogenic nematode (EPN) species due to its favorable ecological and physiological characteristics. Traditionally, this species has been classified as an ambusher based on its host-seeking behavior. However, recent evidence indicates that it is capable of moving considerable distances toward hosts and may exhibit both ambushing and cruising foraging strategies, representing a significant advantage in managing pests inhabiting concealed or cryptic environments.The compatibility of entomopathogenic nematodes with insecticides is of considerable importance for tank-mix or simultaneous applications within integrated pest management (IPM) programs. Metaflumizone is a relatively new insecticide that has been increasingly used worldwide for the management of P. absoluta. The objective of this study was to evaluate the efficacy of the native isolate S. carpocapsae IRMoghan1 against larvae of P. absoluta and to determine its compatibility with metaflumizone. It was hypothesized that S. carpocapsae IRMoghan1 would exhibit cruising-like behavior, enabling it to infect larvae within leaf mines.

 

Method

    Larvae and pupae of P. absoluta were collected from an infested tomato field in Karaj and subsequently reared under greenhouse conditions. Tomato plants were used for insect rearing and bioassays.

First, the compatibility of S. carpocapsae IRMoghan1 with metaflumizone was assessed. A suspension containing 500 infective juveniles (IJs) per milliliter of distilled water was prepared and mixed with 150 mL of metaflumizone solution at the recommended field dose (1000 ppm). A similar IJ suspension in distilled water served as the control. Nematode mortality was recorded at 24, 48, and 72 hours after treatment. The experiment was replicated three times.

To evaluate the effects of the nematode and metaflumizone on P. absoluta larvae, potted tomato plants were placed inside an oviposition cage, and adult moths were released for 24 hours to allow egg laying. The plants were then transferred outside the cage to prevent further infestation. After 72 hours, when egg hatch and larval mine formation were confirmed, mined leaves were used for bioassays.Leaves were sprayed on both surfaces with a nematode suspension at a concentration of 30 IJs per cm², supplemented with Triton X-100 as a surfactant. Control leaves received the same volume of distilled water plus Triton X-100. Treated leaves were detached, and their petioles were placed in narrow 50 mL bottles filled with distilled water to maintain leaf freshness. To evaluate the insecticide effect, tomato plants were sprayed with metaflumizone at concentrations of 1000, 500, and 250 ppm using the same method as for nematode application. All bottles were maintained in a growth chamber at 25°C and approximately 90% relative humidity for 72 hours. Each treatment (including at least 60 larvae) was replicated three times on different days. After 72 hours, leaves were examined under a stereomicroscope, and the numbers of live and dead larvae were recorded. In nematode treatments, dead larvae were dissected to confirm nematode infection. The type of interaction between the nematode and metaflumizone was determined by comparing expected and observed mortality using the method of McVay et al. (1977) and Koppenhöfer and Kaya (1997).

 

Results

    Analysis of variance revealed a significant effect of exposure time on the mortality of infective juveniles treated with metaflumizone (df = 2, 8; F = 4.47; p < 0.05). The lowest nematode mortality (20.53%) was observed 24 hours after treatment, whereas the highest mortality (24.28%) occurred at 72 hours post-treatment. According to IOBC/WPRS classification criteria, metaflumizone was categorized as harmless (Class 1) and compatible with this nematode isolate. Significant differences were observed among treatments regarding larval mortality of P. absoluta (df = 2, 8; F = 11.51; p < 0.001). Based on mean comparisons, metaflumizone at 1000 ppm and S. carpocapsae IRMoghan1 applied alone resulted in the highest larval mortality, whereas metaflumizone at 250 ppm produced the lowest mortality. The calculated interaction parameters indicated an antagonistic interaction between the nematode and metaflumizone.

 

Conclusion

    The compatibility of entomopathogenic nematodes with insecticides for tank-mixing or simultaneous application can reduce application costs and provide economic and environmental benefits. However, compatibility is species- and isolate-specific and must be evaluated prior to combining EPNs with any chemical insecticide. According to IOBC/WPRS classification, metaflumizone was harmless (Class 1) and compatible with S. carpocapsae IRMoghan1. Nevertheless, the observed antagonistic interaction—particularly at lower insecticide concentrations—necessitates further investigation into optimal nematode and insecticide concentrations and appropriate timing for combined application. Overall, the results demonstrated the high virulence of the native isolate S. carpocapsae IRMoghan1 against P. absolutalarvae. According to the host-seeking behavior framework proposed by Lewis et al. (2006), S. carpocapsae is traditionally classified as an ambusher. However, in this study involving P. absoluta larvae, the IRMoghan1 isolate exhibited cruising-like foraging behavior. Since the nematodes were applied to the leaf surface while larvae were feeding within leaf tissues, infective juveniles appeared to follow host-associated cues and penetrate leaf mines to infect the larvae. These findings suggest that host-seeking strategies in entomopathogenic nematodes may be flexible and adaptable to microhabitat conditions and host location, a characteristic that enhances their applicability against diverse pest species.

 

 

 

 

Author Contributions

    Conceptualization, Methodology, Data curation, Formal analysis, Writing, review & editing, Laleh Ebrahimi; Conceptualization and methodological design of the insecticide-related component of the study, Aziz Sheikhi. All authors have read and agreed to the published version of the manuscript.

 

Data availability statement

    Data will be available upon request.

 

Acknowledgements

    This study presents partial results of a project conducted at the Iranian Research Institute of Plant Protection. The authors gratefully acknowledge the support provided by the Iranian Research Institute of Plant Protection and the Karaj Research Station of the Institute.

 

Ethical considerations

    Not applicable.

 

Conflict of interest

     The authors declare that they have no conflict of interest.

منابع

نوزاد، زهرا؛ خانی، سولماز؛ معروف­پور، نریمان و ایرانی پور، شهزاد. (1400). تأثیر باقیمـاندة چند حشـره‌کـش روی لاروهای Tuta absoluta (Lepidoptear: Gelechiidae)  در شرایط آزمایشگاهی.  نامه انجمن حشره شناسی ایران.  41(2), 163-174. https://doi.org/10.22117/jesi.2022.356530.1433
 
REFERENCES
Abbott, W.A. (1925). A method for computing the effectiveness of an insecticide. Journal of Economic Entomology, 18, 265-267.
Abd-Elgawad, M. M. (2023). Optimizing entomopathogenic nematode genetics and applications for the integrated management of horticultural pests. Horticulturae9(8), 865. https://doi.org/10.3390/horticulturae9080865
Alumai, A., & Grewal, P. S. (2004). Tank-mix compatibility of the entomopathogenic nematodes, Heterorhabditis bacteriophora and Steinernema carpocapsae, with selected chemical pesticides used in turfgrass. Biocontrol Science and Technology14(7), 725-730. https://doi.org/10.1080/09583150410001724334
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 absolutaBiocontrol64, 709-721. https://doi.org/10.1007/s10526-019-09973-x
Batalla-Carrera, L., Morton, A., & García-del-Pino, F. (2010). Efficacy of entomopathogenic nematodes against the tomato leafminer Tuta absoluta in laboratory and greenhouse conditions. BioControl55, 523-530. https://doi.org/10.1007/s10526-010-9284-z
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 Nematology35(2),  142.
Desneux, N., Han, P., Mansour, R., Arnó, J., Brévault, T., Campos, M. R., Chailleux, A., Guedes, R.N., Karimi, J., Konan, K.A.J., & Lavoir, A.V. (2022). Integrated pest management of Tuta absoluta: practical implementations across different world regions. Journal of Pest Science, 1-23. https://doi.org/10.1007/s10340-021-01442-8
Chang, P. E. C., & Metz, M. A. (2021). Classification of Tuta absoluta (Meyrick, 1917) (Lepidoptera: Gelechiidae: Gelechiinae: Gnorimoschemini) based on cladistic analysis of morphology. Proceedings of the entomological Society of Washington123(1), 41-54.
Ebrahimi, L., (2023). Efficacy of alginate-based formulation of Steinernema carpocapsae IRMoghan1 against Mythimna loreyi (Lepidoptera: Noctuidae). Biocontrol Science and Technology33(1), 35-47. https://doi.org/10.1080/09583157.2022.2155294
Ebrahimi, L., Niknam, G., & Lewis, E. E. (2011). Lethal and sublethal effects of Iranian isolates of Steinernema feltiae and Heterorhabditis bacteriophora on the Colorado potato beetle, Leptinotarsa decemlineataBioControl56, 781-788. https://doi.org/10.1007/s10526-011-9343-0
Ebrahimi, L., Sheikhigarjan, A., & Ghazavi, M. (2024). Entomopathogenic nematodes for control of potato tuber moth (Phthorimaea operculella [Zeller],(Lepidoptera: Gelechiidae) in infested tubers. International Journal of Pest Management70(4), 1000-1007. https://doi.org/10.1080/09670874.2022.2058709
Ebrahimi, L., TanhaMaafi, Z., & Sharifi, P. (2019). First report of the entomopathogenic nematode, Steinernema carpocapsae, from Moghan region of Iran and its efficacy against the turnip moth, Agrotis segetum Denis and Schiffermuller (Lepidoptera: Noctuidae), larvae. Egyptian Journal of Biological Pest Control 29, 66. https://doi.org/10.1186/s41938-019-0168-y
Garcia-del-Pino, F., Alabern, X., & Morton, A. (2013). Efficacy of soil treatments of entomopathogenic nematodes against the larvae, pupae and adults of Tuta absoluta and their interaction with the insecticides used against this insect. BioControl58, 723-731. https://doi.org/10.1007/s10526-013-9525-z
Georgis, R., & Gaugler, R. (1991). Predictability in biological control using entomopathogenic nematodes. Journal of Economic Entomology, 84(3), 713-720. https://doi.org/10.1093/jee/84.3.713
Husin, T. O. B., & Port, G. R. (2021). Efficacy of entomopathogenic nematodes against Tuta absolutaBiological Control160, 104699. https://doi.org/10.1016/j.biocontrol.2021.104699
Kary, N. E., Sanatipour, Z., Mohammadi, D., & Dillon, A. B. (2021). Combination effects of entomopathogenic nematodes, Heterorhabditis bacteriophora and Steinernema feltiae, with Abamectin on developmental stages of Phthorimaea operculella (Lepidoptera, Gelechiidae). Crop Protection143, 105543. https://doi.org/10.1016/j.cropro.2021.105543
Koppenhöfer, A. M., Cowles, R. S., Cowles, E. A., Fuzy, E. M., & Baumgartner, L. (2002). Comparison of neonicotinoid insecticides as synergists for entomopathogenic nematodes. Biological Control24(1), 90-97. https://doi.org/10.1016/S1049-9644(02)00008-7
Koppenhöfer, A. M., & Kaya, H. K. (1997). Additive and synergistic interaction between entomopathogenic nematodes and Bacillus thuringiensis for scarab grub control. Biological Control8(2), 131-137. https://doi.org/10.1006/bcon.1996.0498
Koppenhöfer, A. M., Shapiro-Ilan, D. I., & Hiltpold, I. (2020). Entomopathogenic nematodes in sustainable food production. Frontiers in Sustainable Food Systems4, 125. https://doi.org/10.3389/fsufs.2020.00125
Kruitbos, L.M., Heritage, S., Hapca, S.M., Wilson, M.J. (2010) The influence of habitat quality on the foraging strategies of the entomopathogenic nematodes Steinernema carpocapsae and Heterorhabditis megidisParasitology137(2), 303-309. https://10.1017/S0031182009991326
Laznik, Ž., & Trdan, S. (2014). The influence of insecticides on the viability of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) under laboratory conditions. Pest Management Science70(5), 784-789. https://doi.org/10.1002/ps.3614
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
Martinez de Altube, M. D. M., Strauch, O., Fernandez De Castro, G., & Martinez Peña, A. (2008). Control of the flat-headed root borer Capnodis tenebrionis (Linné) (Coleoptera: Buprestidae) with the entomopathogenic nematode Steinernema carpocapsae (Weiser) (Nematoda: Steinernematidae) in a chitosan formulation in apricot orchards. BioControl53(3), 531-539. https://doi.org/10.1007/s10526-007-9094-0.
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 Pathology206, 108163. https://doi.org/10.1016/j.jip.2024.108163
Nalinci, E., Karagoz, M., Gulcu, B., Ulug, D., Gulsen, S. H., Cimen, H., Touray, M., David Shapiro-Ilan, D. & Hazir, S. (2021). The effect of chemical insecticides on the scavenging performance of Steinernema carpocapsae: Direct effects and exposure to insects killed by chemical insecticides. Journal of Invertebrate Pathology184, 107641. https://doi.org/10.1016/j.jip.2021.107641
Ndereyimana, A., Nyalala, S., Murerwa, P., & Gaidashova, S. (2020). Field efficacy of entomopathogens and plant extracts on Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) infesting tomato in Rwanda. Crop Protection134, 105183. https://doi.org/10.1016/j.cropro.2020.105183
Nozad, B. Z., Khani, S., Maroofpour, N., & Iranipour, S. (2021). Residual toxicity of some insecticides on Tuta absoluta (Lepidoptera: Gelechiidae) larvae under laboratory conditions. Journal of Entomological Society of Iran, 41(2), 163-174 (In Persian) 
Peters, A. (2003). Pesticides and entomopathogenic nematodes-current status and future work. IOBC WPRS Bulletin26(5), 107-110.
Peters A (1996) The natural host range of Steinernema and Heterorhabditis spp. and their impact on insect populations. Biocontrol Science and Technology, 6(3), 389-402. https://doi.org/10.1080/09583159631361
Roditakis, E., Skarmoutsou, C., & Staurakaki, M. (2013). Toxicity of insecticides to populations of tomato borer Tuta absoluta (Meyrick) from Greece. Pest management science69(7), 834-840. https://doi.org/10.1002/ps.3442
SAS Institute (2012). SAS Enterprise Guide ver. 9.3.
Silva, T. B. M., Silva, W. M., Campos, M. R., Silva, J. E., Ribeiro, L. M. S., & Siqueira, H. A. A. (2016). Susceptibility levels of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) to minor classes of insecticides in Brazil. Crop Protection79, 80-86. https://doi.org/10.1016/j.cropro.2015.10.012
Stuart, R. J., Barbercheck, M. E., Grewal, P. S., Taylor, R. A., & Hoy, C. W. (2006). Population biology of entomopathogenic nematodes: concepts, issues, and models. Biological Control38(1), 80-102. https://doi.org/10.1016/j.biocontrol.2005.09.019
Kaşkavalcı, G., & Türköz, S. (2016). Determination of the efficacy of some entomopathogenic nematodes against Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) under laboratory conditions. Turkish Journal of Entomology40(2). https://doi.org/10.16970/ted.92606
Vainio, A. (1992). Guideline for laboratory testing of the side-effects of pesticides on entomophagous nematodes Steinernema spp. IOBC/WPRS Bulletin, 15, 145–147.
Van Damme, V. M., Beck, B. K., 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 Science72(9), 1702-1709. https://doi.org/10.1002/ps.4195
Wakil, W., Kavallieratos, N. G., Eleftheriadou, N., Yaseen, T., Rasool, K. G., Husain, M., & Aldawood, A. S., 2023. Natural Warriors against Stored-Grain Pests: The Joint Action of Beauveria bassiana and Steinernema carpocapsaeJournal of Fungi, 9(8), 835. https://doi.org/10.3390/jof9080835
Wilson, M.J., Ehlers, R.U., & Glazer, I. (2012) Entomopathogenic nematode foraging strategies–is Steinernema carpocapsae really an ambush forager? Nematology, 14(4),389-94. https://doi.org/10.1163/156854111X617428
White, G.F. (1927). A method for obtaining infective nematode larvae from cultures. Science, 66, 302-303. https://doi.org/10.1126/science.66.1709.302.b
Wu, S. Y., Tang, H., Ban, S., Wen, R., Mao, X., Deng, H., ... & Hou, Y. (2024). Integrated approaches for Solenopsis invicta (Hymenoptera: Formicidae) management: insights from laboratory studies with entomopathogenic nematodes and insecticides. Pest Management Science80(9), 4410-4416. https://doi.org/10.1002/ps.8144