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Effects of storage temperature on viability and virulence of entomopathogenic nematodes Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae), Steinernema carpocapsae Weiser, 1955 and Steinernema feltiae Filipjev, 1934 (Rhabditida: Steinernematidae)

Year 2023, , 247 - 257, 09.10.2023
https://doi.org/10.16970/entoted.1279074

Abstract

Entomopathogenic nematodes (EPN) are a widely used biological control agent. The aim of the study was to detect efficacy and mortalities of some EPN stored at different temperatures and periods. Three EPN species were used in the study. They were Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH hybrid strain, Steinernema carpocapsae Weiser, 1955 TUR-S4 isolate and Steinernema feltiae Weiser, 1955 (Rhabditida: Steinernematidae) TUR-S3 isolate. The species were kept at 4, 15, 25 and 35°C for 7, 14 and 21 days. Subsequently, these species were applied at a dose of 15 Infective juveniles on Tenebrio molitor L., 1758 (Coleoptera: Tenebrionidae) larvae. The study was carried out in laboratory conditions in 2023. As a result, HBH and TUR-S4 kept at 25°C for 14 days and TUR-S3 for 21 days showed the highest virulence as 93.33%. Mortality rates of the EPN species kept at the specified temperatures were also determined. The results have showed that the highest mortality rates for the HBH, TUR-S4 and TUR-S3 isolates were 11.96% on the 14th day at 35°C, 19.81% on the 21st day at 25°C and 7.39% on the 21st day at 35°C, respectively. This study is an important step in determining suitable temperature conditions for storing and transporting EPN.

Supporting Institution

TÜBİTAK

Project Number

219O370

Thanks

This study was financially supported by the TÜBİTAK (The Scientific and Technological Research Council of Türkiye), Project number: 219O370. Moreover, we would like to express our heartfelt thanks to Assoc. Prof. Dr. Hilal SUSURLUK for providing valuable technical support.

References

  • Aryal, S., U. N. Nielsen, N. H. Sumaya, C. Wilson & M. Riegler, 2022. Effect of temperature on survival of Australian entomopathogenic nematodes and their virulence against the Queensland fruit fly, Bactrocera tryoni. BioControl, 67 (6): 617-628.
  • Baimey, H., L. Zadji, L. Afouda, M. Moens & W. Decraemer, 2015. Influence of pesticides, soil temperature and moisture on entomopathogenic nematodes from southern Benin and control of underground termite nest populations. Nematology, 17 (9): 1057-1069.
  • Baker, B. P., T. A. Green & A. J. Loker, 2020. Biological control and integrated pest management in organic and conventional systems. Biological Control, 140: 104095.
  • Barzman, M., P. Bàrberi, E. N. A. Birch, P. Boonekamp, S. Dachbrodt-Saaydeh, B. Graf, B. Hommel, J. E. Jensen, J. Kiss, P. Kudsk, J. R. Lamichhane, A. Messêan, A. C. Moonen, A. Ratnadass, P. Ricci, J. L. Sarah & M. Sattin, 2015. Eight principles of integrated pest management. Agronomy for Sustainable Development, 35 (4): 1199-1215.
  • Boemare, N., C. Laumond & H. Mauleon, 1996. The entomopathogenic nematode-bacterium complex: biology, life cycle and vertebrate safety. Biocontrol Science and Technology, 6 (3): 333-346.
  • Burman, M. & A. E. Pye, 1980. Neoaplectana carpocapsae: Movements of nematode populations on a thermal gradient. Experimental Parasitology, 49 (2): 258-265.
  • Dede, E., A. K. Bütüner, A. Susurluk, 2022. Biocontrol potential of Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH hybrid strain against the beet webworm, Loxostege sticticalis L., 1761 (Lepidoptera: Pyralidae). Turkish Journal of Entomology, 46 (4): 399-405.
  • Dunphy, G. B. & J. M. Webster, 1986. Temperature effects on the growth and virulence of Steinernema feltiae strains and Heterorhabditis heliothidis. Journal of Nematology, 18 (2): 270-272.
  • Ehlers, R. U., 1996. Current and future use of nematodes in biocontrol: practice and commercial aspects with regard to regulatory policy issues. Biocontrol Science and Technology, 6 (3): 303-316.
  • Ehlers, R. U., 2001. Mass production of entomopathogenic nematodes for plant protection. Applied Microbiology and Biotechnology, 56 (5-6): 623-633.
  • El Khoury, Y., M. Oreste, E. Noujeim, N. Nemer & E. Tarasco, 2018. Effect of temperature on the pathogenicity of Mediterranean native entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) from natural ecosystems. Redia, 101 (CI): 123-127.
  • Ewence, A., S. Brescia, I. Johnson & P. C. Rumsby, 2015. An approach to the identification and regulation of endocrine disrupting pesticides. Food and Chemical Toxicology, 78: 214-220.
  • Feng, S. P., R. C. Han, X. H. Qıu, L. I. Cao, J. H. Chen & G. H. Wang, 2006. Storage of osmotically treated entomopathogenic nematode Steinernema carpocapsae. Insect Science, 13 (4): 263-269.
  • Georgis, R., 1992. Present and future prospects for entomopathogenic nematode products. Biocontrol Science and Technology, 2 (2): 83-99.
  • Glazer, I., 1996. Survival mechanisms of entomopathogenic nematodes. Biocontrol Science and Technology, 6 (3): 373-378.
  • Gunnell, D., D. Knipe, S. S. Chang, M. Pearson, F. Konradsen, W. J. Lee & M. Eddleston, 2017. Prevention of suicide with regulations aimed at restricting access to highly hazardous pesticides: a systematic review of the international evidence. The Lancet Global Health, 5 (10): e1026-e1037.
  • Husin, T. O. B. & G. R. Port, 2021. Efficacy of entomopathogenic nematodes against Tuta absoluta. Biological Control, 160: 104699.
  • Iyaniwura, T. T., 1991. Non-target and environmental hazards of pesticides. Reviews on Environmental Health, 9 (3): 161-176.
  • Kaya, H. K. & P. Stock, 1997. “Techniques in Insect Nematology, 281-324”. In: Manual of Techniques in Insect Pathology (Ed. A. Lawrence), Academic Press, 409 pp.
  • 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.
  • Kurtz, B., S. Toepfer, R. U. Ehlers & U. Kuhlmann, 2007. Assessment of establishment and persistence of entomopathogenic nematodes for biological control of western corn rootworm. Journal of Applied Entomology, 131 (6): 420-425.
  • Lu, Y., K. Wu, Y. Jiang, Y. Guo & N. Desneux, 2012. Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature, 487 (7407): 362-365.
  • Nimkingrat, P., S. Khanam, O. Strauch & R. U. Ehlers, 2013. Hybridisation and selective breeding for improvement of low temperature activity of the entomopathogenic nematode Steinernema feltiae. BioControl, 58 (3): 417-426.
  • Özdemir, E., E. Inak, E. Evlice, E. Yüksel, R. A. Delialioğlu & I. A. Susurluk, 2021. Effects of insecticides and synergistic chemicals on the efficacy of the entomopathogenic nematode Steinernema feltiae (Rhabditida: Steinernematidae) against Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Crop Protection, 144: 105605.
  • Rani, L., K. Thapa, N. Kanojia, N. Sharma, S. Singh, A. S. Grewal, A. L. Srivastav & J. Kaushal, 2021. An extensive review on the consequences of chemical pesticides on human health and environment. Journal of Cleaner Production, 283: 124657.
  • Robin, D. C. & P. A. Marchand, 2019. Evolution of the biocontrol active substances in the framework of the European Pesticide Regulation (EC) No. 1107/2009. Pest Management Science, 75 (4): 950-958.
  • Sánchez-Bayo, F., 2012. Insecticides mode of action in relation to their toxicity to non-target organisms. Journal of Environmental and Analytical Toxicology, S4: S4-002.
  • 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.
  • Smits, P. H., 1996. Post-application persistence of entomopathogenic nematodes. Biocontrol Science and Technology, 6 (3): 379-388.
  • Stern, V. M. R. F., R. Smith, R. van den Bosch & K. Hagen, 1959. The integration of chemical and biological control of the spotted alfalfa aphid: the integrated control concept. Hilgardia, 29 (2): 81-101.
  • Strauch, O., I. Niemann, A. Neumann, A. J. Schmidt, A. Peters & R. U. Ehlers, 2000. Storage and formulation of the entomopathogenic nematodes Heterorhabditis indica and H. bacteriophora. BioControl, 45 (4): 483-500.
  • Susurluk, A., R. U. Ehlers, 2008. Field persistence of the entomopathogenic nematode Heterorhabditis bacteriophora in different crops. BioControl, 53 (4): 627-641.
  • Susurluk, I. A. & T.C. Ulu, 2015. Virulence comparisons of high-temperature-adapted Heterorhabditis bacteriophora, Steinernema feltiae and S. carpocapsae. Helminthologia, 52 (2): 118-122.
  • 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.
  • Waage, J. K. & D. J. Greathead, 1988. Biological control: challenges and opportunities. Philosophical Transactions of the Royal Society of London. B, Biological Sciences, 318 (1189): 111-128.
  • Yan, X., M. Shahid Arain, Y. Lin, X. Gu, L. Zhang, J. Li & R. Han, 2020. Efficacy of entomopathogenic nematodes against the tobacco cutworm, Spodoptera litura (Lepidoptera: Noctuidae). Journal of Economic Entomology, 113 (1): 64-72.

Depolama sıcaklığının entomopatojen nematodlar Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae), Steinernema carpocapsae Weiser, 1955 ve Steinernema feltiae Filipjev, 1934 (Rhabditida: Steinernematidae)'nin canlılık ve virülenslikleri üzerine etkileri

Year 2023, , 247 - 257, 09.10.2023
https://doi.org/10.16970/entoted.1279074

Abstract

Entomopatojen nematodlar (EPN) yaygın olarak kullanılan bir biyolojik mücadele ajanıdır. Bu çalışmanın amacı, farklı sıcaklık ve sürelerde depolanan bazı EPN'lerin etkinlik ve ölüm oranlarını belirlemektir. Çalışmada üç EPN türü kullanılmıştır. Bunlar; Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH hibrit ırkı, Steinernema carpocapsae Weiser, 1955 TUR-S4 izolatı ve Steinernema feltiae Weiser, 1955 (Rhabditida: Steinernematidae) TUR-S3 izolatıdır. Bu izolatlar 7, 14 ve 21 gün boyunca 4, 15, 25 ve 35°C'de depolandı. Daha sonra bu türler Tenebrio molitor L., 1758 (Coleoptera: Tenebrionidae) larvaları üzerine 15 Infektif Juvenil dozunda uygulanmıştır. Çalışma, 2023 yılında laboratuvar koşullarında yapılmıştır. Sonuç olarak; HBH ve TUR-S4 25°C'de 14 gün, TUR-S3 ise 21 gün süreyle %93,33 ile en yüksek virülans göstermiştir. Ayrıca, aynı sıcaklıklarda tutulan EPN türlerinde ölüm oranları da belirlenmiştir. Sonuçlar, HBH, TUR-S4 ve TUR-S3 izolatları için en yüksek ölüm oranlarının sırasıyla 35°C'de 14. günde %11,96, 25°C'de 21. günde %19,81 ve 35°C'de 21. günde %7,39 olduğunu göstermiştir. Bu çalışma, EPN'nin depolanması ve nakliyesi sırasında uygun sıcaklık koşullarının belirlenmesinde önemli bir adımdır.

Project Number

219O370

References

  • Aryal, S., U. N. Nielsen, N. H. Sumaya, C. Wilson & M. Riegler, 2022. Effect of temperature on survival of Australian entomopathogenic nematodes and their virulence against the Queensland fruit fly, Bactrocera tryoni. BioControl, 67 (6): 617-628.
  • Baimey, H., L. Zadji, L. Afouda, M. Moens & W. Decraemer, 2015. Influence of pesticides, soil temperature and moisture on entomopathogenic nematodes from southern Benin and control of underground termite nest populations. Nematology, 17 (9): 1057-1069.
  • Baker, B. P., T. A. Green & A. J. Loker, 2020. Biological control and integrated pest management in organic and conventional systems. Biological Control, 140: 104095.
  • Barzman, M., P. Bàrberi, E. N. A. Birch, P. Boonekamp, S. Dachbrodt-Saaydeh, B. Graf, B. Hommel, J. E. Jensen, J. Kiss, P. Kudsk, J. R. Lamichhane, A. Messêan, A. C. Moonen, A. Ratnadass, P. Ricci, J. L. Sarah & M. Sattin, 2015. Eight principles of integrated pest management. Agronomy for Sustainable Development, 35 (4): 1199-1215.
  • Boemare, N., C. Laumond & H. Mauleon, 1996. The entomopathogenic nematode-bacterium complex: biology, life cycle and vertebrate safety. Biocontrol Science and Technology, 6 (3): 333-346.
  • Burman, M. & A. E. Pye, 1980. Neoaplectana carpocapsae: Movements of nematode populations on a thermal gradient. Experimental Parasitology, 49 (2): 258-265.
  • Dede, E., A. K. Bütüner, A. Susurluk, 2022. Biocontrol potential of Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH hybrid strain against the beet webworm, Loxostege sticticalis L., 1761 (Lepidoptera: Pyralidae). Turkish Journal of Entomology, 46 (4): 399-405.
  • Dunphy, G. B. & J. M. Webster, 1986. Temperature effects on the growth and virulence of Steinernema feltiae strains and Heterorhabditis heliothidis. Journal of Nematology, 18 (2): 270-272.
  • Ehlers, R. U., 1996. Current and future use of nematodes in biocontrol: practice and commercial aspects with regard to regulatory policy issues. Biocontrol Science and Technology, 6 (3): 303-316.
  • Ehlers, R. U., 2001. Mass production of entomopathogenic nematodes for plant protection. Applied Microbiology and Biotechnology, 56 (5-6): 623-633.
  • El Khoury, Y., M. Oreste, E. Noujeim, N. Nemer & E. Tarasco, 2018. Effect of temperature on the pathogenicity of Mediterranean native entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) from natural ecosystems. Redia, 101 (CI): 123-127.
  • Ewence, A., S. Brescia, I. Johnson & P. C. Rumsby, 2015. An approach to the identification and regulation of endocrine disrupting pesticides. Food and Chemical Toxicology, 78: 214-220.
  • Feng, S. P., R. C. Han, X. H. Qıu, L. I. Cao, J. H. Chen & G. H. Wang, 2006. Storage of osmotically treated entomopathogenic nematode Steinernema carpocapsae. Insect Science, 13 (4): 263-269.
  • Georgis, R., 1992. Present and future prospects for entomopathogenic nematode products. Biocontrol Science and Technology, 2 (2): 83-99.
  • Glazer, I., 1996. Survival mechanisms of entomopathogenic nematodes. Biocontrol Science and Technology, 6 (3): 373-378.
  • Gunnell, D., D. Knipe, S. S. Chang, M. Pearson, F. Konradsen, W. J. Lee & M. Eddleston, 2017. Prevention of suicide with regulations aimed at restricting access to highly hazardous pesticides: a systematic review of the international evidence. The Lancet Global Health, 5 (10): e1026-e1037.
  • Husin, T. O. B. & G. R. Port, 2021. Efficacy of entomopathogenic nematodes against Tuta absoluta. Biological Control, 160: 104699.
  • Iyaniwura, T. T., 1991. Non-target and environmental hazards of pesticides. Reviews on Environmental Health, 9 (3): 161-176.
  • Kaya, H. K. & P. Stock, 1997. “Techniques in Insect Nematology, 281-324”. In: Manual of Techniques in Insect Pathology (Ed. A. Lawrence), Academic Press, 409 pp.
  • 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.
  • Kurtz, B., S. Toepfer, R. U. Ehlers & U. Kuhlmann, 2007. Assessment of establishment and persistence of entomopathogenic nematodes for biological control of western corn rootworm. Journal of Applied Entomology, 131 (6): 420-425.
  • Lu, Y., K. Wu, Y. Jiang, Y. Guo & N. Desneux, 2012. Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature, 487 (7407): 362-365.
  • Nimkingrat, P., S. Khanam, O. Strauch & R. U. Ehlers, 2013. Hybridisation and selective breeding for improvement of low temperature activity of the entomopathogenic nematode Steinernema feltiae. BioControl, 58 (3): 417-426.
  • Özdemir, E., E. Inak, E. Evlice, E. Yüksel, R. A. Delialioğlu & I. A. Susurluk, 2021. Effects of insecticides and synergistic chemicals on the efficacy of the entomopathogenic nematode Steinernema feltiae (Rhabditida: Steinernematidae) against Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Crop Protection, 144: 105605.
  • Rani, L., K. Thapa, N. Kanojia, N. Sharma, S. Singh, A. S. Grewal, A. L. Srivastav & J. Kaushal, 2021. An extensive review on the consequences of chemical pesticides on human health and environment. Journal of Cleaner Production, 283: 124657.
  • Robin, D. C. & P. A. Marchand, 2019. Evolution of the biocontrol active substances in the framework of the European Pesticide Regulation (EC) No. 1107/2009. Pest Management Science, 75 (4): 950-958.
  • Sánchez-Bayo, F., 2012. Insecticides mode of action in relation to their toxicity to non-target organisms. Journal of Environmental and Analytical Toxicology, S4: S4-002.
  • 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.
  • Smits, P. H., 1996. Post-application persistence of entomopathogenic nematodes. Biocontrol Science and Technology, 6 (3): 379-388.
  • Stern, V. M. R. F., R. Smith, R. van den Bosch & K. Hagen, 1959. The integration of chemical and biological control of the spotted alfalfa aphid: the integrated control concept. Hilgardia, 29 (2): 81-101.
  • Strauch, O., I. Niemann, A. Neumann, A. J. Schmidt, A. Peters & R. U. Ehlers, 2000. Storage and formulation of the entomopathogenic nematodes Heterorhabditis indica and H. bacteriophora. BioControl, 45 (4): 483-500.
  • Susurluk, A., R. U. Ehlers, 2008. Field persistence of the entomopathogenic nematode Heterorhabditis bacteriophora in different crops. BioControl, 53 (4): 627-641.
  • Susurluk, I. A. & T.C. Ulu, 2015. Virulence comparisons of high-temperature-adapted Heterorhabditis bacteriophora, Steinernema feltiae and S. carpocapsae. Helminthologia, 52 (2): 118-122.
  • 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.
  • Waage, J. K. & D. J. Greathead, 1988. Biological control: challenges and opportunities. Philosophical Transactions of the Royal Society of London. B, Biological Sciences, 318 (1189): 111-128.
  • Yan, X., M. Shahid Arain, Y. Lin, X. Gu, L. Zhang, J. Li & R. Han, 2020. Efficacy of entomopathogenic nematodes against the tobacco cutworm, Spodoptera litura (Lepidoptera: Noctuidae). Journal of Economic Entomology, 113 (1): 64-72.
There are 36 citations in total.

Details

Primary Language English
Subjects Nematology
Journal Section Articles
Authors

Alperen Kaan Bütüner 0000-0002-2121-3529

Merve İlktan 0009-0007-9999-5034

Alper Susurluk 0000-0002-0699-1752

Project Number 219O370
Early Pub Date October 7, 2023
Publication Date October 9, 2023
Submission Date April 7, 2023
Acceptance Date September 12, 2023
Published in Issue Year 2023

Cite

APA Bütüner, A. K., İlktan, M., & Susurluk, A. (2023). Effects of storage temperature on viability and virulence of entomopathogenic nematodes Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae), Steinernema carpocapsae Weiser, 1955 and Steinernema feltiae Filipjev, 1934 (Rhabditida: Steinernematidae). Turkish Journal of Entomology, 47(3), 247-257. https://doi.org/10.16970/entoted.1279074
AMA Bütüner AK, İlktan M, Susurluk A. Effects of storage temperature on viability and virulence of entomopathogenic nematodes Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae), Steinernema carpocapsae Weiser, 1955 and Steinernema feltiae Filipjev, 1934 (Rhabditida: Steinernematidae). TED. October 2023;47(3):247-257. doi:10.16970/entoted.1279074
Chicago Bütüner, Alperen Kaan, Merve İlktan, and Alper Susurluk. “Effects of Storage Temperature on Viability and Virulence of Entomopathogenic Nematodes Heterorhabditis Bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae), Steinernema Carpocapsae Weiser, 1955 and Steinernema Feltiae Filipjev, 1934 (Rhabditida: Steinernematidae)”. Turkish Journal of Entomology 47, no. 3 (October 2023): 247-57. https://doi.org/10.16970/entoted.1279074.
EndNote Bütüner AK, İlktan M, Susurluk A (October 1, 2023) Effects of storage temperature on viability and virulence of entomopathogenic nematodes Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae), Steinernema carpocapsae Weiser, 1955 and Steinernema feltiae Filipjev, 1934 (Rhabditida: Steinernematidae). Turkish Journal of Entomology 47 3 247–257.
IEEE A. K. Bütüner, M. İlktan, and A. Susurluk, “Effects of storage temperature on viability and virulence of entomopathogenic nematodes Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae), Steinernema carpocapsae Weiser, 1955 and Steinernema feltiae Filipjev, 1934 (Rhabditida: Steinernematidae)”, TED, vol. 47, no. 3, pp. 247–257, 2023, doi: 10.16970/entoted.1279074.
ISNAD Bütüner, Alperen Kaan et al. “Effects of Storage Temperature on Viability and Virulence of Entomopathogenic Nematodes Heterorhabditis Bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae), Steinernema Carpocapsae Weiser, 1955 and Steinernema Feltiae Filipjev, 1934 (Rhabditida: Steinernematidae)”. Turkish Journal of Entomology 47/3 (October 2023), 247-257. https://doi.org/10.16970/entoted.1279074.
JAMA Bütüner AK, İlktan M, Susurluk A. Effects of storage temperature on viability and virulence of entomopathogenic nematodes Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae), Steinernema carpocapsae Weiser, 1955 and Steinernema feltiae Filipjev, 1934 (Rhabditida: Steinernematidae). TED. 2023;47:247–257.
MLA Bütüner, Alperen Kaan et al. “Effects of Storage Temperature on Viability and Virulence of Entomopathogenic Nematodes Heterorhabditis Bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae), Steinernema Carpocapsae Weiser, 1955 and Steinernema Feltiae Filipjev, 1934 (Rhabditida: Steinernematidae)”. Turkish Journal of Entomology, vol. 47, no. 3, 2023, pp. 247-5, doi:10.16970/entoted.1279074.
Vancouver Bütüner AK, İlktan M, Susurluk A. Effects of storage temperature on viability and virulence of entomopathogenic nematodes Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae), Steinernema carpocapsae Weiser, 1955 and Steinernema feltiae Filipjev, 1934 (Rhabditida: Steinernematidae). TED. 2023;47(3):247-5.

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